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CRUSTACEAN BIOENERGETICS: MITOCHONDRIAL ADAPTIVE MOLECULAR RESPONSES TO FACE ENVIRONMENTAL CHALLENGES.

INTRODUCTION: THE EVOLUTIONARY HISTORY OF CRUSTACEANS AND THEIR IMPORTANCE IN THE STUDY OF MITOCHONDRIAL FUNCTION

Crustaceans are one of the most diverse groups of invertebrate animals; the subphylum includes up to 17,635 species (De Grave et al. 2009). Some crustaceans have an ancient origin and a large evolutionary history based on limited paleontological evidence which is not well understood, not only because scientific efforts are limited, but also because of the highly diverse environments inhabited by these species.

To date, fossil evidence including the identification of a 520 million-y-old fossil of Ercaia, which was one of the earliest crustaceans ever found, suggests that crustaceans originated during the middle Cambrian (Chen et al. 2001). Marine crustaceans appeared during the Paleozoic, when some species such as the currently extinct Carpopenaeus spp., occurred (Rehm et al. 2011), then freshwater species, including the crayfish families such as Astacidae, Cambaridae. and Parastacidae, emerged much later, after the first terrestrial arthropods conquered land during the Silurian [443 to 419 million years ago (mya)], and are assumed to have their monophyletic origins during the Triassic period (185 to 22 mya) before Pangea split (Crandall et al. 2000). Finally, the existence of the first terrestrial crustaceans. Isopods, was confirmed by fossil record during the Cretaceous period (145 to 66 mya, Broly et al. 2013).

Although some million-year gaps make unclear the freshwater-species origin, the ability of crustaceans to successfully invade new environments is clear (Glenner et al. 2006). The abilities reproduction in both aerial and aquatic environments point toward the presence of adapted subcellular components, such as mitochondria. These organelles appeared on earth much earlier than animals, around 2.000 mya (during the Precambrian). when changing levels of atmospheric oxygen seem to have driven the mitochondrial evolution in species whose energetic needs promoted the origin of new molecules and highly specialized metabolic pathways (Lane 2002).

Crustacean diversity is represented through their highly specialized morphological and physiological characteristics. Some species may be found in highly extreme environments, where extensive physiological adaptations are required to ensure survival. For example, the amphipods Apherusa glacialis and Gammarus wilkitzkii, which inhabit the Arctic sea ice, possess physiological strategies to survive low temperatures, cope with food scarcity, and their metabolic rates are adapted to an energy-saving lifestyle (Poltermann et al. 2000. Werner & Auel 2005).

Parasitic crustaceans are also interesting species as they can infect a wide range of marine and freshwater invertebrates and vertebrates, mainly fish (Smit et al. 2014). Copepods, isopods. and brachyuran species show an amazing variety of adaptations, including the ability to redirect all the reproductive energy from a host through a process termed "host castration." which allows parasitic species to use and control the host energy, behavior, and physiology (Laffcrly & Kuris 2009). Of relevance also are the energetic mechanisms of low-oxygen tolerant species, such as the brine shrimp Artemia franciscana, whose quiescent embryos respond to long-term anoxia through down-regulation of metabolic processes and cessation of the transcription of mitochondrial proteins (Kwast & Hand 1996. Eads& Hand 2003). In addition, a number of various shrimp and lobster species have shown migratory behavior throughout their life cycle, which exposes them to highly variable environmental conditions (Dall et al. 1990).

At this point, bioenergetics, defined as the series of biological processes involved in energy flow and its chemical transformation, become central when studying mitochondrial genes and proteins, their function, and regulatory mechanisms to control energy expenditure, as well as the physiological response to environmental changes. Furthermore, it should be noted that mitochondria play also a central role in the generation of byproducts known as reactive oxygen species (ROS) and in their control through the activation of antioxidant systems and during the initiation of cell apoptosis. These processes are still scarcely understood in crustacean's mitochondria, and this knowledge will be helpful to researchers when trying to elucidate the abilities of crustaceans to regulate their energetic balance, which determines the degree of fitness and species perpetuation.

Fortunately, during the past decade, an increasing number of studies have focused on understanding the biology of crustaceans such as shrimp, lobsters and crabs, which are the most studied species because of their commercial values. In this review, we summarize the knowledge concerning crustacean bioenergetics, mitochondrial genes, and proteins and, specifically, the physiological response of mitochondria to environmental changes such as hypoxia. We also summarize current information regarding the transition permeability phenomenon and the presence of alternative enzymes in their respiratory chain or alternative sources and mechanisms to produce adenosine triphosphate (ATP).

CRUSTACEAN MITOGENOMES AND THE SHRIMP TRANSCRIPTOME

During the past three decades, the study of crustacean biology has increased considerably, and the use of novel techniques and tools has provided a better understanding of the biology of these species. Although only one crustacean nuclear genome data set has been published to date (the waterflea Daphnia pulex, Colbourne et al. 2011), the mitochondrial genomes (mitogenomes or mtDNAs) of several crustacean species reported to date have provided valuable information for establishing their evolutionary history, their phylogenetic relationships, and patterns of gene flow between species (Wilson et al. 2000).

To our knowledge, Artemia franciscana was the first crustacean species whose mtDNA was reported (Valverde et al. 1994). The total length of the A. franciscana mtDNA is 15.N22 base pairs (bp), a similar size to the mtDNA of insects such as the fly Drosophila yakuba (16,019 bp, Clary & Wolstenholme 1985) and the bee Apis metlifera (16,343 bp, Crozier & Crozier 1993). Some other crustacean mtDNAs have also been reported, including those of the waterflea Daphnia pulex (Crease 1999), the tiger shrimp Penaeus monodon (Wilson et al. 2000), the copepod Tigriopus japonicus (Machida et al. 2002), the Japanese blue crab Portunus trituberculatus (Yamauchi et al. 2003), and the freshwater crab Geothelphusa dehaani (Segawa & Aotsuka 2005). To date, there are more than a hundred reported mtDNAs from crustaceans, including 86 from Malacostracans, which is the largest of the six classes of crustaceans and includes extinct and living species, such as shrimp, lobsters, crabs, krill. mantis, and crayfish (Shen et al. 2015). The mtDNA sequences of all these species include the 13 mitochondrial-eneoded proteins, although some genes appear in different arrangements or include unusual characteristics, which are species specific (Kilpert & Podsiadlowski 2006). These 13 mitochondrial proteins encode subunits constituting the mitochondrial multimeric complexes involved in the electron transport chain and oxidative phosphorylation (Staton et al. 1997, Shen et al. 2007). Among crustaceans, shrimp, because of its commercial importance, are some of the most widely studied species. Particularly, the Pacific whiteleg shrimp Litopenaeus vannamei, whose mtDNA was reported in 2007 by Shen et al, will be considered as a key species in this review.

Besides mitogenomes. during the last 10y, molecular biology advances have led to the sequencing of transcriptomes (nuclear and mitochondrial transcripts) of an increasing number of crustaceans, which also provide a major source of information to better understand the mitochondrial machinery.

It is well known that in addition to the mitochondrial-eneoded proteins, most mitochondrial multimeric complexes from the respiratory chain require a series of nuclear-encoded proteins, which are imported from the cytosol to the mitochondria, to assemble the active complex.

In this review, the expressed sequence tags of some nuclear transcripts encoding mitochondrial proteins were selected from the Litopenaeus vannamei transcriptome database (Ghaffari et al. 2014) and their deduced proteins analyzed. Table 1 shows a summary of some of those shrimp proteins that may play central roles within the mitochondria, including those from metabolic pathways such as the Krebs cycle, the electron transport chain, and ATP synthesis.

All the transcripts analyzed in Table 1 were blasted against the National Center for Biotechnology Information (NCBI) database using BLASTx and compared with protein sequences from other animal species available in the GenBank database. No mtDNA-encoded proteins were included in the analysis because they were previously reported by Shen et al. (2007). The analyzed proteins include the complex I or NADH dehydrogenase subunits, the A and B subunits of complex II or succinate dehydrogenase, and various subunits of complex III or cytochrome bcl. The analyzed subunits of complex IV or cytochrome c oxidase (COX) included only proteins whose transcripts have not been reported to date. Previously, some of the full-length COX transcripts were sequenced and characterized such as: COX4 (GenBank accession no. JQ828862.1), COX5A (GenBank accession no. JQ839284.1), COX5B (GenBank accession no. JQ952564.1) (Jimenez-Gutierrez et al. 2013), and COX6A (GenBank accession no. KF906252.1), COX6B (GenBank accession no. KF906253.1) and COX6C (GenBank accession no. KF906254.1) (Mendez-Romero 2014); also their genes expressions have been analyzed.

Many deduced proteins encoding complex V or ATP-synthasc subunits are included in Table 1 along with the nuclear encoded ATP9 (GenBank accession no. EU194608.1, Muhlia-Almazan et al. 2008), and the main nuclear-encoded subunits from the F, domain of ATP synthase such as subunits ATP[alpha] (GenBank accession no. GQ848643.3), ATP[beta] (GenBank accession no. GQ848644.1), ATPy (GenBank accession no. HM036579.1), ATP[delta] (GenBank accession no. HM036580.1), and ATP[epsilon] (GenBank accession no. HM036581.1, Martinez-Cruz et al. 2011. Martinez-Cruz et al. 2015). The previously reported ATPase inhibitory protein IF, (GenBank accession no. KF306266.1) was not included in Table 1, although it is a central regulatory protein which has been associated with the ATP hydrolysis regulatory mechanism of shrimp mitochondria (Faccenda & Campanella 2012, Chimeo et al. 2015).

Table 1 also includes other important deduced proteins found in the shrimp transcriptome, such as those previously reported in mammals to act as regulatory proteins and those that may play a role during the permeability transition (PT) of the mitochondrial membrane; these include voltage dependent anion channel, cyclophilin D, the phosphate carrier protein, and the adenine nucleotide translocator (Bernardi 2013).

Data in Table 1 contain a comparison of the shrimp-deduced proteins with the homologous proteins from other marine invertebrates, including crustaceans as the copepods Tigriopus californicus and Lepeophtheirus salmonis, the crayfish Marsupenaeus japonicus, the water flea Daphnia pulex, the crab Eriocheir sinensis, and several species of molluscs (Lingula anatina, Crassostrea gigas, Biomphalaria glabrata, and Aplysia californica). In addition, it is important to point out the high similarities detected between crustacean and insect protein sequences. This finding is in agreement with the analysis previously described in phylogenetic studies from different mitochondrial shrimp proteins which suggests the existence of a shared common ancestor, Pancrustacea, of Crustacea and insects (Regier et al. 2010, Chimeo et al. 2015, Martinez-Cruz et al. 2015).

MITOCHONDRIAL RESPONSES TO OXIDATIVE STRESS AND ROS PRODUCTION IN CRUSTACEANS

Mitochondria, considered the powerhouse of the cell, produce ATP from adenosine diphosphate and inorganic phosphate through a coupled mechanism. The ATP synthesis involves a series of electron transport reactions in the inner mitochondrial membrane, where oxygen is an essential component to facilitate the oxidation of substrates that ultimately allows ATP production (Mitchell 1966, Boyer 1997).

In the aquatic environment, oxygen is less available to organisms than it is in the air. During shrimp adult and early stages, at the open sea, small variations are detected in the water oxygen levels; however, after postlarvae migration to low deep refuge zones as estuaries, or even in the culture ponds, oxygen levels may vary continuously from normoxia during daytime to hypoxia at night (Puente-Carreon 2009, Fig. 1).

Thus, water-breathers have fixed adaptive mechanisms to obtain this valuable molecule, even in those extreme environments with very low dissolved oxygen concentrations, and maintain the mitochondrial machinery functions. Indeed, the availability of molecular oxygen determines the adaptive ability of some species to face the stress produced by low [O.sub.2] concentrations, and the damage that increased ROS produces (Guzy & Schumacker 2006, Welker et al. 2013).

The Effect of Hypoxia on the Mitochondrial Function of Crustaceans

In marine ecosystems, the transitory fluctuations in oxygen concentration may lead to death in unadapted marine species (Vaquer-Sunyer & Duarte 2008). The physiological responses of individual species to changes in the environmental oxygen concentration may help to distinguish those marine animals that tolerate anoxia/hypoxia from those which are sensitive.

Whereas sensitive organisms use energy compensatory pathways, tolerant species instead use energy conservatory mechanisms to maintain their energy balance (Gorr et al. 2006). In the presence of low oxygen levels, unadapted or hypoxia-sensitive organisms display physiological responses that stimulate specific metabolic pathways to increase ATP production, and under such condition, there is a marked shift from aerobic to anaerobic metabolism. Hypoxia-sensitive animals also show a quick decay in cellular ATP concentration, causing activation of proteases, an uncontrolled rise in the concentration of calcium ions, continuous membrane depolarization, and cell death under low oxygen conditions (Lutz & Milton 2004, Nilsson & Lutz 2004). On the other hand, animals adapted to hypoxia maintain normal ATP levels by entering a reversible hypometabolic state, in which pathways consuming ATP are repressed in the presence of restricted oxygen availability (Boutilier 2001, Hochachka & Lutz 2001, Storey 2004). In addition, some of these species may store large glycogen reserves in their tissues, are able to activate powerful antioxidant systems, and may possess mitochondrial enzymes, such as alternative oxidases (AOX) and uncoupling proteins (UCP) that may help to control ROS formation (Lutz & Nilsson 1997, Hermes-Lima & Zenteno-Savin 2002, Sokolova & Sokolov 2005, Abele et al. 2007).

Various shrimp species are thought to be hypoxia-sensitive because low oxygen levels may affect their mitochondrial functions (Wu et al. 2002, Sun et al. 2015); however, some anoxia-adapted species, such as Artemia franciscana, have developed interesting strategies to survive prolonged periods of anoxia, many of which are, presumably, tightly related to their mitochondrial adaptations (Menze et al. 2005).

Recent studies have focused on the mitochondrial responses of crustaceans after exposure to hypoxia and re-oxygenation events. At the transcriptional level, hypoxia significantly affects the expression of various nuclear-encoded mitochondrial proteins (Jimenez-Gutierrez et al. 2014, Martinez-Cruz et al. 2015). The hypoxia-inducible factor (HIF) has been identified as the main regulator of the transcriptional responses to hypoxia in mammalian mitochondria. This transcription factor with a heterodimeric structure comprised an oxygen-regulated a subunit (HIF-[alpha]), and a constitutively expressed [beta] subunit (Semenza 2000) is translocated to the nucleus during hypoxia, where it binds to specific DNA sequences to regulate a large number of genes implicated in energetic metabolism, including 6-phosphofructo-2-kinase, fructose-2,6-biphosphatase 3 and 4, and COX subunits 4-1 (Minchenko et al. 2003, Fukuda et al. 2007). In crustaceans. HIF has been characterized only in a few species, including Litopenaeus vannamei, Palaemonetes pugio, Daphnia magna, and Callinectes sapidus, and its ability to control a variety of cellular and systematic homeostatic responses to hypoxic stress has been partially confirmed (Gorr et al. 2004, Li & Brouwer 2007, Sonanez-Organis et al. 2009, Hardy et al. 2012).

Recently, new high-throughput sequencing technologies have been used to examine the effects of hypoxia on the transcriptome of some crustaceans, including the red swamp crayfish (Procambarus clarkii), the oriental river prawn (Macrobrachium nipponense), and the white shrimp (Litopenaeus vannamei). The results indicated an increase in the expression of genes encoding proteins implicated in the mobilization of carbohydrates and lipids, downregulation of genes involved in the protein degradation machinery, and no major changes in genes encoding proteins of the translational machinery after exposure to hypoxia (Shen et al. 2014, Johnson et al. 2015, Sun et al. 2015).

The transcripts of some nuclear-encoded proteins from the mitochondrial respiratory chain of the shrimp Litopenaeus vannamei are known to be downregulated by hypoxia, including some proteins that compose the Frcatalytic domain of the ATP synthase (Martinez-Cruz et al. 2015), the regulatory [IF.sub.1] mitochondrial protein that inhibits ATPase activity (Chimeo et al. 2015), and some nuclear-encoded subunits of the COX complex (Jimenez-Gutierrez et al. 2013).

In addition to transcriptional changes, several other biochemical and physiological alterations have been observed in shrimp-isolated mitochondria in response to hypoxia/re-oxygenation. The synthesis of mitochondrial proteins, mainly those that are part of the COX and ATP synthase complexes, were significantly affected by the dissolved oxygen concentration of seawater (Martinez-Cruz et al. 2012, Jimenez-Gutierrez et al. 2014), and lower levels of proteins such as ATP[beta] and COX1 (the catalytic subunits of mitochondrial complexes IV and V) have been observed under hypoxic conditions when compared with normoxia. Also, COX activity and the oxygen consumption of muscle-isolated mitochondria significantly decrease under hypoxia (Jimenez-Gutierrez et al. 2014).

Opposite to other enzymes, the mitochondrial ATPase activity of Litopenaeus vannamei increased during hypoxia (Martinez-Cruz et al. 2012), an adaptation that was suggested to maintain the membrane potential and cellular homeostasis, as previously observed in vertebrate species. It has been proposed that in shrimp muscle, the presence of arginine-phosphate may act as a buffer to maintain the tissue ATP levels during hypoxia. As previously mentioned, shrimp may face daily hypoxia/re-oxygenation cycles throughout their lifetime, and these events may be analogous to the oxidative stress that ischemia/reperfusion episodes can provoke in well-studied vertebrate models (Abele et al. 2012). In fact, re-oxygenation, which is the abrupt increase in the oxygen concentration after hypoxia, seriously affects mitochondrial function in invertebrates because of an increase in ROS production, which may provoke profound cellular damage (Hermes-Lima & Zenteno-Savin 2002, Solaini & Harris 2005). Previous studies have confirmed that shrimp rapidly respond to increasing oxygen levels after hypoxia by reducing ATPase activity and ATP levels. Furthermore, the activities of mitochondrial enzymes, such as citrate-synthase and COX, which are downregulated during hypoxia, increase abruptly (Martinez-Cruz et al. 2012, Jimenez-Gutierrez et al. 2014). At re-oxygenation. white shrimp are able to restore their mitochondrial functions to those observed at normoxia; however, recent findings suggest that many of the biochemical responses observed at re-oxygenation as the L-lactate levels in plasma may return to the previous levels after 12-24 h of re-oxygenation, as observed in L. vannamei (Chimeo et al., submitted).

These findings suggest that shrimp mitochondria have the ability to conform to changes in environmental oxygen availability because their oxygen consumption rate increases/decreases in direct relation with the dissolved oxygen levels (data not shown), supporting the hypothesis that shrimp species are not as sensitive to hypoxia as previously suggested. Future studies, however, are required to fully understand, at the organelle level, how shrimp mitochondrial enzymes deal with continuous fluctuations in the dissolved oxygen concentration of seawater and to elucidate the strategies these species use to control mitochondrial ROS production under these conditions, besides the activation of their antioxidant system.

ROS Production and Mitochondrial Responses to Oxidative Stress in Crustaceans

Oxidative stress results in an increase in the production of ROS, mainly as byproducts during mitochondrial electron transport. The oxygen radical superoxide ([O.sup.*-.sub.2]) and hydrogen peroxide ([H.sub.2][O.sub.2]) are commonly produced during normal oxidative metabolism. It has been established that an excessive production of ROS has been associated with a range of pathological conditions that may result in tissue and cell damage (Kowaltowski et al. 2009). Those aquatic species that cyclically encounter broad changes in dissolved oxygen concentration may cope with the damage caused to cell proteins, lipids, and nucleic acids by an overproduction of ROS (Lawniczak et al. 2013).

Some crustaceans have shown an increase in lipids peroxidation in response to oxidative stress brought on by episodes of hypoxia/anoxia. In 2005, de Oliveira et al. used the lipids peroxidation assay (thiobarbituric acid reactive substances, TBARS) to demonstrate that lipid peroxidation significantly increases in the gills of the estuarine crab Chasmagnathus granulate during anoxia recovery. In addition, during air exposure (when intertidal crabs are not in seawater), lipids peroxidation occurs in various crustacean tissues, including the hepatopancreas, muscle, anterior and posterior gills of crab species such as Callinectes danae and Callinectes ornatus as a response to the oxidative damage caused by ROS (Freire et al. 2011).

In addition to lipid peroxidation, protein carbonyl groups produced as a result of oxidative protein damage have been detected in hepatopancreas, muscle, and gills of crustaceans such as the stone crab (Paralomis granulosa) after 24 h of air exposure (Romero et al. 2007); thus, damage signals in lipids and proteins are a consequence of ROS accumulation in the mitochondria after hypoxia/anoxia. Nevertheless, certain organs in some marine invertebrates, such as the hepatopancreas of the snail Littorina littorea (Hermes-Lima & Zenteno-Savin 2002), and muscle, hepatopancreas, and gills of the white shrimp Litopenaeus vannamei (Zenteno-Savin et al. 2006), are unaffected by anoxia and do not demonstrate lipid peroxidation after hypoxia. This lack of lipid and protein damage by ROS has been suggested to be organ-dependent and may be related to several factors, including the duration of hypoxia/anoxia/re-oxygenation exposure, the antioxidant capacity of the specific organ/tissue, and/or species-specific mitochondrial mechanisms that may control ROS generation.

In crustaceans, the increase in mitochondrial ROS production during hypoxia/re-oxygenation acts as a signal that triggers cellular responses that initially include activation of the antioxidant systems, both enzymatic (superoxide dismutase, catalase, glutathione-peroxidase, and peroxiredoxin) and non-enzymatic (vitamins C, E, thiamine, and glutathione) molecules that are known to be induced and modulated by many factors, including oxygen deprivation, the presence of heavy metal ions, pathogen infection, and ammonia stress. The extent of activation of these antioxidant systems varies throughout the life cycle in crustaceans (Aispuro-Hernandez et al. 2008, Parrilla-Taylor & Zenteno-Savin 2011, Abele et al. 2012). At this point, a new central question emerges; besides the activation of antioxidant systems, do crustacean mitochondria have another mechanism(s) to deal with the increased ROS production stimulated by hypoxic/re-oxygenation conditions?

The Mitochondrial Uncoupling Mechanisms of Crustaceans and Other Marine Invertebrates

The mitochondrial electrochemical gradient, or proton motive force ([DELTA][p.sub.m]), is generated through the electron transport chain and used by the ATP synthase to produce ATP. This [DELTA][p.sub.m] involves two components: an electrical constituent denoted as the mitochondrial transmembrane potential ([DELTA][PSI]) and a chemical constituent, the pH difference across the mitochondrial inner membrane (MIM) (Mitchell 1966, Sanderson et al. 2013).

Besides the [DELTA][PSI] role in ATP synthesis, it is also involved in the production of ROS because an increased [DELTA][PSI] is known to slow electron transfer among the enzymes in the respiratory chain; intermediates react allowing a single electron reduction of oxygen, this produces an electron scape and superoxide anion formation, which is then converted to other ROS (Murphy 2009).

Within the mitochondria, [DELTA][PSI] tends to increase during nutrient oxidation and decreases during oxidative phosphorylation or mitochondrial uncoupling. This allows the uncoupling of ATP synthesis from the proton electrochemical gradient via a proton leak into the mitochondrial matrix, promoting a decreased [DELTA][PSI] without ATP production (Slocinska et al. 2011). To date, various studies have confirmed that ROS production can be controlled by regulating [DELTA][PSI] (Drose & Brandt 2012), and the mitochondrial uncoupling mechanisms have been suggested to prevent a high [DELTA][PSI] (Kowaltowski et al. 2009).

The uncoupling mechanisms that may be linked to the high resistance of some species to reoxygenation-derived oxidative stress by reducing ROS production include: 1) proton sinks that involve the UCP, the bacterial mitochondrial unspecific channels, or the PT pore (PTP) of mammals; and 2) the non-pumping alternative redox enzymes including a NADH-dehydrogenase type 2 (NDH2), the mitochondrial glycerol-3-phosphate-dehydrogenase (mtGPDH), and the AOX, each as an additional participant in a branched respiratory chain (Kadenbach 2003, Lesser 2006, Guerrero-Castillo et al. 2011).

The UCP are mitochondrial carrier proteins located in the inner membrane, and considered uncouplers, because these proteins are capable of dissociating ATP synthesis from the respiratory chain by dissipating the proton gradient. This protein family includes a core group of five mammalian UCP variants (UCP 1-5), which are differentially expressed in a tissue-specific manner (Chan et al. 2006, Bermejo-Nogales et al. 2014).

In the last decade, the number of studies of invertebrate UCP has risen. Various studies have reported at least two UCP--UCP4 and UCP5--in the mitochondria of invertebrates, including parasites such as the nematode Caenorhabditis elegans (UCP4), insects such as the fruit fly Drosophila melanogaster (UCP4), the blood sucking insect Rhodnius prolixus (UCP4), and the cockroach Gromphadorhina cocquereliana. These studies have suggested that UCP4 is involved in regulating lipid metabolism and/or in protecting against oxidative stress (Slocinska et al. 2011. Ji et al. 2012, Alves-Bezerra et al. 2014. Da-Re et al. 2014). To date, the eastern oyster Crassostrea virginica (UCP5) is the only marine mollusc in which the presence of UCP has been demonstrated (Kern et al. 2009). Recently, our research group has confirmed the existence of UCP4 and UCP5 in the white shrimp mitochondria (Mendez-Romero 2016).

The Mitochondrial Permeability Transition Enigma in Crustaceans

The physiological uncoupling ability of mitochondria is closely related to the inner membrane PT. This phenomenon, which results from the opening of the mitochondrial unspecific channel in bacteria, has been confirmed in mammals and in some yeasts such as Saccharomyces cerevisiae and Debaryomyces hansenii (Cabrera-Orefice et al. 2010, Guerrero-Castillo et al. 2011). In mammalian mitochondria, PT reflects an increased permeability of the MIM that results from stress conditions which promote an intracellular calcium imbalance accompanied by elevated phosphate concentrations and adenine nucleotide reduction (Halestrap et al. 1998). The long-lasting PT enables the free passage of protons and molecules less than 1.5 kDa in size into the mitochondrial matrix; as a result, the proton barrier disappears, and the [DELTA][p.sub.m] is no longer preserved (Halestrap 2009. Bernardi 2013).

It has been well established that mitochondrial PT can be triggered by anoxia/hypoxia and ischemia/reperfusion events, as well as pathological conditions that may induce apoptosis (Bernardi et al. 2006, Menze et al. 2010). This response was first assumed to be mediated by the opening of a multiprotein channel or pore, which induces mitochondrial swelling, membrane depolarization, uncoupled respiration, and if prolonged, leads to the rupture of the outer mitochondrial membrane, the release of cytochrome c, and, ultimately, apoptosis of the cell (Kroemer et al. 2007, Giorgio et al. 2013).

To date, scarce information is available about the ability of crustacean mitochondria to undergo PT (Menze et al. 2010). Early studies in the mitochondria from Artemia franciscana embryos suggested the existence of the three main proteins forming the mitochondrial pore: the voltage dependent-anion channel (VDAC), the adenine nucleotide translocator (ANT), and the mitochondrial cyclophilin D (Cyp D) as it was first suggested for the mammalian mitochondrial pore (Halestrap & Davidson 1990, Menze et al. 2005); however, the high calcium loads that promote those responses observed in mammalian mitochondria were not detected in Artemia; therefore, the existence of a non-calcium regulated pore in this species was suggested (Menze et al. 2005). Mitochondria from other crustaceans including the ghost shrimp Lepidophthalmus louisianensis (Holman & Hand 2009) and the northern shrimp Crangon crangon and Palaemon serratus (Konrad et al. 2012) have been studied, and the compiled evidence suggests that crustacean mitochondria lack the ability to induce a PT in response to a cellular calcium increase.

In 2010, Menze et al., suggested this non-calcium-regulated pore may be specific to arthropods because no PT was detected in the mitochondrial membrane of the oyster Crassostrea virginica (Sokolova et al. 2004); however, von Stockum et al. (2015) recently reported that, similar to mammals, the mitochondria from Drosophila melanogaster have a [Ca.sup.2+]-induced [Ca.sup.2+] release channel (mCrC) that shares regulatory features with the PTP and opens in a [Ca.sup.2+]-induced manner. To our knowledge, these findings suggest that in crustaceans, mitochondria PT may not be regulated, or at least not regulated by [Ca.sup.2+], but instead by another ion (Krumschnabel et al. 2005).

In fact, inhibition or resistance of crustacean mitochondria to induced PT may represent a mechanism for depressing apoptosis, as suggested by Menze et al. (2010); however, the regulation of apoptosis in crustaceans is currently not well understood, and future experiments are required to more fully examine the function of the mitochondrial PTP in crustaceans and to ultimately support or reject this hypothesis.

The Alternative Mitochondrial Enzymes of Marine Invertebrates

An additional mitochondrial uncoupling strategy may involve the participation of various alternative respiratory enzymes. which may be present in the mitochondrial apparatus. These non-pumping enzymes are part of a branched respiratory chain and transfer electrons from one enzyme to the next one without pumping protons from the mitochondrial matrix to the inter-membrane space, thereby differing from the classical transport chain, and promoting a decreased [DELTA][PSI] and ROS generation (McDonald et al. 2009).

To date, an alternative type-2 NADH dehydrogenase (NADH2), a mitochondrial glycerol-3-phosphate dehydrogenase (mtGPDH), and an AOX are the three enzymes reported as part of the mitochondrial branched respiratory chains of mammals, yeast, and marine invertebrates (Abele et al. 2007, Mracek et al. 2013). The NADH2 serves as an alternative to the multisubunit respiratory complex I, and catalyzes the transfer of electrons from NADH to ubiquinone in the mitochondrial respiratory chain. In yeast, the NADH2 oxidizes NADH on the matrix side and reduces ubiquinone to maintain mitochondrial NADH/NAD(+) homeostasis without generating an electrochemical gradient (Feng et al. 2012). This enzyme may be found mainly in bacteria, yeast, fungi, and Arabidopsis thaliana, but not in mammals or arthropods (Iwata et al. 2012). There are currently no reports of the presence of these enzymes in crustaceans or other invertebrate marine organisms.

The mtGPDH is the smallest protein found in the mammalian respiratory chain (74 kDa). This enzyme is located on the outer side of the MIM, is FAD-dependent, and has been suggested to be a major source of ROS production in the mitochondrial intermembrane space. The function of mtGPDH has largely been discussed in mammals and invertebrates such as the fruit fly Drosophda melanogaster; the enzyme may act as part of the mitochondrial electron transport chain by transferring electrons to ubiquinone and acting as an uncoupling mechanism susceptible to proton leak (Miwa et al. 2003, Vrbacky et al. 2007, Carmon & Maclntyre 2010). Among invertebrates, an mtGPDH was localized in the mitochondria of the parasites Trypanosoma brucei and Leishmania major (Skodova et al. 2013), but to date there are no reports confirming the existence of this enzyme in crustaceans.

The AOX, also known as ubiquinol oxidase, catalyzes the oxidation of ubiquinol and the reduction of four electrons from molecular oxygen to water; it is alternative to the COX function but without pumping protons to the intermembrane space, insensitive to cyanide, and is located in the MIM. In mammals, AOX prevents an over-reduction of ubiquinone, and a consequent overproduction of superoxide (El-Khoury et al. 2013). In marine invertebrates, such as annelid worms, sipunculid worms, and molluscs, the presence of an AOX has been described; nevertheless, to date there are no reports of this enzyme in crustaceans (McDonald et al. 2009).

In 2007, Abele et al., suggested that when the mitochondrial respiratory rate of some marine invertebrate hypoxia-tolerant species, including the bivalve Arctica islandica, decreases under disadvantageous conditions, the mitochondrial AOX may help to maintain the mitochondrial respiratory rate without disturbing the energetic balance of cells. In addition, AOX may also exhibit an antioxidant function by minimizing ROS formation. Recently, Sussarellu et al. (2012) detected a significant increase in expression of the AOX transcripts of the Pacific giant oyster Crassostrea gigas during re-oxygenation, and confirmed this increase as a protective mechanism against the abrupt increase in ROS production.

Crustacean mitochondria possess some peculiarities when compared with other related groups. There are presently no published studies examining mitochondrial uncoupling mechanisms in crustaceans. So far, new evidence resulting from the identification of specific mitochondrial transcripts and proteins, and the determination of mitochondrial responses from various crustacean species, suggests the existence of putative AOX (data not shown) and UCP in decapods (Mendez-Romero 2016). Further research in this area is needed to confirm the functionality of these enzymes and proteins, its participation in the mitochondrial antioxidant defense, and to correlate its function with the ability of some crustacean species to tolerate hypoxia/anoxia and avoid ROS production.

CRUSTACEAN PHYSIOLOGICAL PROCESSES, IONS TRANSPORT, AND ATP PRODUCTION

Although a considerable number of studies have described in great detail, the transport of specific ions such as calcium and sodium in the mitochondria of vertebrate cells, studies on these ions transport mechanisms in crustaceans are still limited. In vertebrates, calcium plays essential roles in regulating the mitochondrial volume and the regulatory activities of some calcium-dependent enzymes in the Krebs cycle. In fact, as previously discussed in The Mitochondrial Permeability Transition Enigma in Crustaceans, various calcium-dependent transport mechanisms may directly influence mitochondrial functions and cell death (Bernardi 1999, Campanella et al. 2004).

In crustaceans, calcium is not only required to complete basic cellular functions but has also been shown to be essential for meeting energetic demands during growth and molting (Zilli et al. 2003, 2007). The role of calcium in crustacean hepato-pancreatic cells has also been studied, and calcium has been determined to participate in regulating the concentration of heavy metals, including copper, zinc, iron, and magnesium, which play important roles in enzymes activation and in the synthesis of respiratory pigments such as hemocyanin. At higher concentrations, such metal ions become toxic, and a regulatory mechanism involving mitochondrial heavy-metal sequestration has been suggested in the mitochondria of epithelial hepatopancreatic cells from species such as the American lobster Homarus americanus. It has been proposed that this mechanism involves a calcium-heavy metal uniporter uptake that transports divalent cations from the cytoplasm to the mitochondria, where an insoluble nontoxic precipitate is accumulated (Chavez-Crooker et al. 2001, 2002, Ahearn et al. 2004).

To date, there is no information about the mitochondrial carrier proteins involved in the [Ca.sup.2+] flux of crustaceans; however, new published information about the transcriptome of species such as Litopenaeus vannamei (Ghaffari et al. 2014) confirmed the existence of various expressed sequence tags encoding mitochondrial proteins that participate in the calcium in- and out-fluxes. The existence of the mitochondrial [Ca.sup.2+] uniporter, which dynamically buffers physiological [Ca.sup.2+] concentrations in mitochondria, has been confirmed in this shrimp species (data not shown); however, to date there is no information that confirms the existence of proteins such as calcium antiporters either 2[N.sub.a+] or 2[H.sub.+] in crustaceans. Future studies are needed to better understand the extensive ability of shrimp mitochondria to uptake high calcium concentrations without suffering the mitochondrial PT phenomenon as it happens in all other species mitochondria.

ATP Production from Sulfide

In the 1930s it was first reported that some organisms are able to survive in the presence of sulfide, despite the fact that environments with high sulfide contents also have low dissolved oxygen concentrations in water, thus promoting anoxic or hypoxic marine conditions. To survive under these harsh environmental conditions, organisms have developed adaptive strategies, including the ability to cover their bodies and internal epithelial mucosa with sulfide-oxidizing bacteria (Grieshaber & Volkel 1998). In addition, early studies have suggested that mitochondria present in gills of the gutless clam Solemya reidi may convert sulfide into less toxic compounds and produce energy in a coupled reaction to synthesize ATP (Powell & Somero 1986).

Later, O'Brien and Vetter (1990) suggested that the mitochondrial electron transport chain complexes contribute to ATP production from sulfide and estimated that mitochondria of Solemya reidi produce approximately 2.0-3.2 ATP molecules per sulfide molecule. More than two decades later, Hildebrandt and Grieshaber (2008) proposed a mechanism to explain mitochondrial oxidation of sulfide in the lugworm Arenicola marina, which produces thiosulfate, a less toxic compound, and the simultaneous electron transfer from sulfide oxidation to the respiratory chain complexes III and IV. During this process, for each pair of electrons, six protons are translocated from the intermembrane space to the mitochondrial matrix and 1.5 ATP molecules are synthesized (Hinkle 2005).

Presently, three enzymes are known to be involved in the sulfide conversion and ATP production. The first enzyme is sulfide:quinone oxidoreductase, which is located in the MIM where it oxidizes sulfide ([H.sub.2]S) to persulfide (R-SSH) and transfers two electrons to the ubiquinone pool, as described by Theissen and Martin (2008). The second and third enzymes--a sulfur dioxygenase that achieves four-electron oxidation of one persulfide molecule to sulfite in the presence of oxygen and water, and a sulfur transferase, which transfers a sulfite to persulfide, resulting in the production of thiosulfate--are located in the mitochondrial matrix (Hildebrandt & Grieshaber 2008, Fig. 2).

Some additional studies have focused on the ability of species to tolerate high-sulfide concentrations, and the use of sulfide as a substrate to produce ATP have been found in crustaceans such as the shrimp species Calocaris macandreae, Callianassa subterranea, and Jaxea nocturna (Johns et al. 1997). In 2001, Bourgeois and Felder confirmed that mitochondria isolated from the ghost shrimp Lepidophthalmus louisianensis under high-sulfide and hypoxic conditions are able to synthesize ATP at a rate of 0.474-14.750 nmol ATP/min/mg protein. Furthermore, the thiosulfate levels increased in the hemolymph of these organisms during exposure to anoxic-sulfide water. Therefore, the authors suggested that ATP production from thiosulfate occurs in mitochondria through the electromotive force, which is generated by the electron/proton donor reaction between sulfide and thiosulfate (Bourgeois & Felder 2001). It seems that, in certain species, prolonged exposure to sulfide has allowed mitochondria to adapt their functions to include the production of ATP from this alternative energy source.

CONCLUDING REMARKS

The central role of mitochondria in cellular bioenergetics has been reviewed extensively elsewhere. This organelle directly uses oxygen to produce energy, and it inevitably produces toxic byproducts known as ROS. Although previous information provides some evidence on the way crustaceans have adapted to hypoxia, early studies focused on understanding the mitochondrial functions of these species seem to indicate diverse specific regulatory responses, which may lead future research to better understand their abilities to surpass the marine environment continuous variations, maintaining their bio-energetic equilibrium.

As previously discussed, the Pacific whiteleg shrimp, now suggested as a hypoxia-tolerant species, may enter into a reversible hypometabolic state when oxygen availability is low. At this condition, the genie expression of specific nuclear-encoded mitochondrial subunits from the respiratory chain is down-regulated and the hydrolytic activity of central enzymes as the mitochondrial ATPase is regulated through an [IF.sub.1] protein that may control ATP expenditure and the ATP levels of shrimp mitochondria decrease as a consequence of a prolonged lactate production even in the presence of oxygen during re-oxygenation. Under oxidative stress conditions, the antioxidant system of shrimp is well known to rapidly respond to the increasing ROS production; however, the existence and functionality of mitochondrial uncoupling mechanisms such as alternative enzymes and UCPs, are being studied and their ability to protect crustacean cells remains to be confirmed. In addition, it remains to be determined whether the existence and function of uncoupling mechanisms in mitochondria confer the ability to shrimp to efficiently face hypoxia/re-oxygenation cycles. In some other well-studied animal models, the ability of mitochondria to uncouple has been associated to the inner membrane PT. Nevertheless, previous studies suggest that crustacean mitochondria lack the capacity to undergo PT; this may also explain the resistance of shrimp mitochondria to hypoxia/re-oxygenation damage.

Several central questions regarding the mitochondrial functions in crustaceans remain unanswered. Does the PT phenomenon exist in crustacean mitochondria? What induces or regulates the PT in the inner mitochondrial membrane of crustaceans? How do shrimp mitochondria regulate calcium transport? Does hypoxia affect the calcium in- and out-flow in shrimp mitochondria? As many mitochondrial enzymes are multimeric complexes that participate as a whole in the energy-producing pathways, a central task to solve is the identification of all those proteins and subunits forming part of complexes, and regulatory mechanisms in crustaceans because there is clear evidence that confirms the existence of species-specific proteins that may accomplish new regulatory functions.

ACKNOWLEDGMENTS

AMA and OMC acknowledge support from Consejo Nacional de Ciencia y Tecnologia (CON ACyT) and graduate scholarships to CC and CMR. This work was supported by Consejo Nacional de Ciencia y Tecnologia (grant 241670).

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OLIVIERT MARTINEZ-CRUZ, (1) CINDY CHIMEO, (2) CHRYSTIAN M. RODRIGUEZ-ARMENTA (2) AND ADRIANA MUHLIA-ALMAZAN (2*)

(1) Departamento de Investigation y Posgrado en Alimentos, Universidud de Sonora, Boulevard Luis Encinas SjN. Col. Centra, Hermosillo, Sonora 83000, Mexico; 'Bioenergetics and Molecular Genetics Lab, Centro de Investigation en Alimentation y Desarrollo A.C. Carretera a la Victoria km 0.6, Hermosillo, Sonora 1735, Mexico

(*)Corresponding author. E-mail: amuhlia@ciad.mx

DOI: 10.2983/35.036.0327
TABLE 1.
The deduced proteins of nuclear-encoded transcripts involved in the
mitochondrial function of the white shrimp Litopenaeus vannamei.

                                             Similar to other
                                             Crustaceans transcripts
                                             or expressed
                                             sequence tags
Deduced protein name from                    (GenBank access no.)
L. vannamei transcripts

Electron transport chain complex I
NADH dehydrogenase subunit F                   L. vannamei
                                               FEI01646.1
                                               -
NADH dehydrogenase                             Penaeus monodon
[ubiquinone] flavoprotein 2
                                               GE615804.1
                                               -
NADH dehydrogenase                             L. vannamei
[ubiquinone] flavoprotein 3
                                              FE 126620.1
                                               -
NADH dehydrogenase                             L. vannamei
[ubiquinone] 1 beta subcomplex
subunit 4                                      FE053783.1
                                               -
NADH dehydrogenase                             No record
[ubiquinone] 1 alpha subcomplex
subunit 5                                      -
                                               -
NADH dehydrogenase                             No record
[ubiquinone] 1 alpha subcomplex
subunit 6                                      -
                                               -
NADH dehydrogenase                             P. monodon
[ubiquinone] iron-sulfur protein 7
                                               GW995271.1
                                               -
NADH dehydrogenase                             P. monodon
[ubiquinone] 1 alpha subcomplex
subunit 8                                      EE662014.1
                                               -
NADH dehydrogenase                             L. vannamei
[ubiquinone] 1 alpha subcomplex
subunit 9                                      FE185623.1
                                               -
NADH dehydrogenase                             L. vannamei
[ubiquinone] 1 alpha subcomplex
subunit 11                                     FE156411.1
                                               -
NADH dehydrogenase                             No record
[ubiquinone] 1 alpha subcomplex
subunit 12                                     -
                                               -
Electron transport chain complex II
Succinate dehydrogenase subunit A              L. vannamei
                                               FE050092.1
                                               -
Succinate dehydrogenase subunit B              L. vannamei
                                               FE103086.1
                                               -
Electron transport chain
complex III
Cytochrome b5                                  L. vannamei
                                               FE126775.1
                                               -
Cytochrome b-cl complex subunit Rieske         L. vannamei
                                              FE 154972.1
                                               -
Cytochrome b-cl complex subunit 1              L. vannamei
                                               FE103284.1
                                               -
Cytochrome b-cl complex subunit 2              P. monodon
                                               GW995086.1
                                               -
Cytochrome b-cl complex subunit 7              L. vannamei
                                               FE150813.1
                                               -
Cytochrome cl                                  P. monodon
                                               GO073581.1
                                               -
Electron transport chain
complex IV
Cytochrome c                                   L. vannamei
                                               FE126543.1
                                               -
COX 7 subunit A                                L. vannamei
                                               FE153349.1
                                               -
COX 11                                         L. vannamei
                                               FE075323.1
                                               -
COX 15                                         P. monodon
                                               GE615894.1
                                               -
COX 16                                         P. monodon
                                               GW996288.1
Electron transport
chain complex V
ATP synthase subunit D                         L. vannamei
                                               FE123815.1
                                               -
ATP synthase subunit E                         L. vannamei
                                               GR973479.1
                                               -
ATP synthase subunit F                         L. vannamei
                                               FE137182.1
                                               -
ATP synthase subunit G                         Fenneropenaeus indicus
                                               GT968440.1
                                               -
ATP synthase subunit O                         L. vannamei
                                               FE157827.1
                                               -
Krebs cycle
Citrate synthase                               L. vannamei
                                               FE103408.1

Aconitase                                      L. vannamei
                                               FE135452.1
                                               -
Succinyl-CoA synthetase                        L. vannamei
subunit alpha
                                               FE076651.1
                                               -
ADP-forming Succinyl-CoA                       L. vannamei
ligase subunit beta
                                               FE051092.1
                                               -
Mitochondrial NADP(+)-dependent                L. vannamei
Isocitrate dehydrogenase
                                               FE107598.1
                                               -
Mitochondrial NAD(+)-Isocitrate                L. vannamei
dehydrogenase subunit alpha
                                               CK572301.1
                                               -
Mitochondrial NAD(+)-Isocitrate                L. vannamei
dehydrogenase subunit beta
                                               FE061769.1
                                               -
Mitochondrial NAD(+)-Isocitrate                L. vannamei
dehydrogenase subunit gamma
                                              FE 174200.1
                                               -
Malate dehydrogenase                           L. vannamei
                                               FE123204.1
                                               -
Fumarase                                       No record
                                               -
                                               -
2-Oxoglutarate dehydrogenase                   L. vannamei
                                               FE178128.1
                                               -
Dihydrolipoyllysine-residue                    P. monodon
succinyltransferase
                                               GE615760.1
                                               -
Pyruvate dehydrogenase complex
Pyruvate dehydrogenase El                      L. vannamei
component subunit alpha
                                               FE085445.1
                                               -
Pyruvate dehydrogenase El                      Metapenaeus ensis
component subunit beta
                                               CV179091.1
                                               -
Dihydrolipoyllysine-residue                    P. monodon
acetyltransferase
                                               GE616028.1
                                               -
Dihydrolipoyl dehydrogenase                    P. monodon
                                               GE615629.1
                                               -
Mitochondrial carriers, permeability
transition, and calcium transport proteins
Voltage-dependent anion channel                L. vannamei
                                               FE102731.1
                                               -
Adenine nucleotide                             P. monodon
translocator isoform 3
                                               GW995486.1
                                               -
Cyclophilin D                                  L. vannamei
                                               FE087681.1
                                               -
Phosphate carrier protein                      L. vannamei
                                               FE149241.1
                                               -

                                                 Similar to other
Deduced protein name from                        species proteins:
L. vannamei transcripts

Electron transport chain complex I
NADH dehydrogenase subunit F                   Aplysia californica
                                               Komagataeibacter
                                               intermedins TF2
                                               Rhizopus delemar
                                               RA 99-880
NADH dehydrogenase                             Paramecium tetraurelia
[ubiquinone] flavoprotein 2                    strain d4-2
                                               Tetrahymena thermophila
                                               SB2I0
                                               Salpingoeca rosetta
NADH dehydrogenase                             Acyrthosiphon pisum
[ubiquinone] flavoprotein 3
                                               Peromyscus maniculatus
                                               hairdii
                                               Rattus norvegicus
NADH dehydrogenase                             Zootermopsis nevadensis
[ubiquinone] 1 beta subcomplex
subunit 4                                      Diaphorina cilri
                                               Sparus aurata
NADH dehydrogenase                             Camelina saliva
[ubiquinone] 1 alpha subcomplex
subunit 5                                      Zootermopsis nevadensis
                                               Brassica rapa
NADH dehydrogenase                             Phoenix dactylifera
[ubiquinone] 1 alpha subcomplex
subunit 6                                      Jatropha curcas
                                               Brassica rapa
NADH dehydrogenase                             Zootermopsis nevadensis
[ubiquinone] iron-sulfur protein 7
                                               Plutella xylostella
                                               Danaus plexippus
NADH dehydrogenase                             Zootermopsis nevadensis
[ubiquinone] 1 alpha subcomplex
subunit 8                                      Bactrocera dorsalis
                                               Drosophila melanogaster
NADH dehydrogenase                             Ichthyophthirius
[ubiquinone] 1 alpha subcomplex                multifiliis
subunit 9                                      Solanum lycopersicum
                                               Tarenaya hassleriana
NADH dehydrogenase                             Bactrocera cucurbitae
[ubiquinone] 1 alpha subcomplex
subunit 11                                     Ceratitis capitata
                                               Musca domestica
NADH dehydrogenase                             Tetrahymena thermophila
[ubiquinone] 1 alpha subcomplex                SB210
subunit 12                                     Ichthyophthirius
                                               multifiliis
                                               Stylonychia lemnae
Electron transport chain complex II
Succinate dehydrogenase subunit A              Paramecium tetraurelia
                                               strain d4-2
                                               Tetrahymena thermophila
                                               SB210
                                               Moesziomyces antarclicus
                                               T-34
Succinate dehydrogenase subunit B              Zootermopsis nevadensis
                                               Lysiphlebus testaceipes
                                               Anopheles darlingi
Electron transport chain
complex III
Cytochrome b5                                  Tribolium castaneum
                                               Zootermopsis nevadensis
                                               Anopheles darlingi
Cytochrome b-cl complex subunit Rieske         Tribolium castaneum
                                               Culex quinquefasciatus
                                               Oreochromis niloticus
Cytochrome b-cl complex subunit 1              Homo sapiens
                                               Pongo abelii
                                               Tarsius syrichta
Cytochrome b-cl complex subunit 2              Tribolium castaneum
                                               Acromyrmex echinatior
                                               Salmo salar
Cytochrome b-cl complex subunit 7              Musca domestica
                                               Ceratitis capitata
                                               Bactrocera dorsalis
Cytochrome cl                                  Tetrahymena thermophila
                                               Stylonychia lemnae
                                               Oxytricha trifallax
Electron transport chain
complex IV
Cytochrome c                                   Marsupenaeus japonicus
                                               Tigriopus californicus
                                               Locusta migratoria
COX 7 subunit A                                Zootermopsis nevadensis
                                               Musca domestica
                                               Bactrocera cucurbitae
COX 11                                         Bactrocera cucurbitae
                                               Ceratitis capitata
                                               Culex quinquefasciatus
COX 15                                         Culex quinquefasciatus
                                               Anopheles darlingi
                                               Danio rerio
COX 16                                         Tribolium castaneum
                                               Zootermopsis nevadensis
                                               Bombyx mori
Electron transport
chain complex V
ATP synthase subunit D                         Solenopsis invicta
                                               Bombus terreslris
                                               Anopheles darlingi
ATP synthase subunit E                         Aedes albopictus
                                               Apis mellijera
                                               Ceratitis capilata
ATP synthase subunit F                         Anopheles darlingi
                                               Culex quinquefasciatus
                                               Aedes aegypti
ATP synthase subunit G                         Palaemon varians
                                               Ixodes scapularis
                                               Musca domestica
ATP synthase subunit O                         Coptotermes formosanus
                                               Linepithema humile
                                               Tribolium caslaneum
Krebs cycle
Citrate synthase                               Anopheles darlingi
                                               Sus scrofa
                                               Danio rerio
Aconitase                                      Lasius niger
                                               Daphnia magna
                                               Daphnia pulex
Succinyl-CoA synthetase                        Anopheles darlingi
subunit alpha
                                               Culex quinquefasciatus
                                               Zootermopsis nevadensis
ADP-forming Succinyl-CoA                       Riptortus pedestris
ligase subunit beta
                                               Zootermopsis nevadensis
                                               Tribolium castaneum
Mitochondrial NADP(+)-dependent                Zootermopsis nevadensis
Isocitrate dehydrogenase
                                               Salmo salar
                                               Astyanax mexicanus
Mitochondrial NAD(+)-Isocitrate                Crassostrea gigas
dehydrogenase subunit alpha
                                               Strongyloides ratti
                                               Aplysia californica
Mitochondrial NAD(+)-Isocitrate                Musca domestica
dehydrogenase subunit beta
                                               Bombyx mori
                                               Linepithema humile
Mitochondrial NAD(+)-Isocitrate                Tribolium caslaneum
dehydrogenase subunit gamma
                                               Diaphorina citri
                                               Harpegnathos saltator
Malate dehydrogenase                           Ictalurus pune talus
                                               Danio rerio
                                               Daphnia pulex
Fumarase                                       Tribolium castaneum
                                               Zootermopsis nevadensis
                                               Danio rerio
2-Oxoglutarate dehydrogenase                   Apis mellifera
                                               Bomhus terrestres
                                               Tribolium castaneum
Dihydrolipoyllysine-residue                    Culex quinquefasciatus
succinyltransferase
                                               Bombyx mori
                                               Musca domestica
Pyruvate dehydrogenase complex
Pyruvate dehydrogenase El                      Tetrahymena thermophila
component subunit alpha                        SB210
                                               Oxytricha trifallax
                                               Euplotes sp. BB-2004
Pyruvate dehydrogenase El                      Zootermopsis nevadensis
component subunit beta
                                               Danio rerio
                                               Apis mellifera
Dihydrolipoyllysine-residue                    Crassostrea gigas
acetyltransferase
                                               Lingula anatina
                                               Biomphalaria glabrata
Dihydrolipoyl dehydrogenase                    Zootermopsis nevadensis
                                               Rhy-opertha dominica
                                               Tribolium castaneum
Mitochondrial carriers, permeability
transition, and calcium transport proteins
Voltage-dependent anion channel                Eriocheir sinensis
                                               Culex quinquefasciatus
                                               Anopheles darlingi
Adenine nucleotide                             Poecilia Formosa
translocator isoform 3
                                               Stegastes partitus
                                               Cynoglossus semilaevis
Cyclophilin D                                  Poecilia Formosa
                                               Larimichthys crocea
                                               Danio rerio
Phosphate carrier protein                      Lingula anatina
                                               Stegodyphus mimosarum
                                               Crassostrea gigas

                                                  GenBank
Deduced protein name from                         access no.    Total
L. vannamei transcripts                                         score

Electron transport chain complex I
NADH dehydrogenase subunit F                    XP_005097475.1     170
                                                    GAN86293.1     170
                                                    EIE75829.1     170
NADH dehydrogenase                              XP 001347081.1     298
[ubiquinone] flavoprotein 2
                                                XP_001017531.1     279
                                                XP_004990429.1     226
NADH dehydrogenase                              XP_003240259.1      47.4
[ubiquinone] flavoprotein 3
                                                XP_006973964.1      43.5
                                                   NP_072129.2      40.8
NADH dehydrogenase                                  KDR12405.1     138
[ubiquinone] 1 beta subcomplex
subunit 4                                       XP_008477125.1     112
                                                    AGV76785.1      77.4
NADH dehydrogenase                              XP_010442830.1      50.4
[ubiquinone] 1 alpha subcomplex
subunit 5                                           KDR17347.1      45.1
                                                XP_009119817.1      49.7
NADH dehydrogenase                              XP_008775040.1      57.8
[ubiquinone] 1 alpha subcomplex
subunit 6                                       XP_012068683.1      57.4
                                                XP 009120779.1      55.1
NADH dehydrogenase                                 KDR 14423.1     300
[ubiquinone] iron-sulfur protein 7
                                                XP_011549720.1     292
                                                    EHJ72892.1     288
NADH dehydrogenase                                  KDR15899.1     223
[ubiquinone] 1 alpha subcomplex
subunit 8                                       XP_011202093.1     214
                                                   NP_611954.2     207
NADH dehydrogenase                              XP_004034899.1     280
[ubiquinone] 1 alpha subcomplex
subunit 9                                       XP_004247128.1     169
                                                XP_010548735.1     169
NADH dehydrogenase                              XP_011196653.1     129
[ubiquinone] 1 alpha subcomplex
subunit 11                                      XP_004522669.1     124
                                                XP_005179354.1      98.6
NADH dehydrogenase                              XP_001471372.1     152
[ubiquinone] 1 alpha subcomplex
subunit 12                                      XP_004027195.1     138
                                                    CDW76573.1     127
Electron transport chain complex II
Succinate dehydrogenase subunit A               XP_001347005.1     452
                                                XP_001014703.2     447
                                                    GAC72599.1     444
Succinate dehydrogenase subunit B                   KDR22350.1     449
                                                    AAY63983.1     435
                                                    ETN61683.1     424
Electron transport chain
complex III
Cytochrome b5                                      XP_975884.1     369
                                                    KDR21019.1     352
                                                    ETN57924.1     342
Cytochrome b-cl complex subunit Rieske          NP_001164310.1     328
                                                XP_001867379.1     322
                                                XP_003447114.1     319
Cytochrome b-cl complex subunit 1                  NP_003356.2      99.8
                                                XP_009237316.1      99.8
                                                XP_008066364.1      98.2
Cytochrome b-cl complex subunit 2                  XP_975769.1     315
                                                XP_011059867.1     302
                                                   ACN 10092.1     287
Cytochrome b-cl complex subunit 7               XP_005181276.1     120
                                                XP_004529599.1     117
                                                XP_011198166.1     115
Cytochrome cl                                   XP_001027842.2     407
                                                    CDW90024.1     270
                                                    EJY73104.1     266
Electron transport chain
complex IV
Cytochrome c                                        BAJ22990.1     202
                                                    AAC80550.1     186
                                                    AGF80276.1     185
COX 7 subunit A                                   K.DR 19493.1      70.1
                                                XP_005188857.1      62.8
                                                XP_011178340.1      59.7
COX 11                                          XP_011188067.1     326
                                                XP_004522467.1     320
                                                XP_001865568.1     311
COX 15                                          XP_001868025.1     466
                                                    ETN60022.1     463
                                                    AAH66452.1     409
COX 16                                             XP_972022.1      97.1
                                                    KDR21754.1      84.7
                                                XP_004929682.1      80.1
Electron transport
chain complex V
ATP synthase subunit D                          XP_011161901.1     352
                                                XP_003397933.1     343
                                                    ETN66668.1     335
ATP synthase subunit E                              AAV90734.1      82.4
                                                   XP_624249.1      79.7
                                                XP_004524140.1      73.6
ATP synthase subunit F                              ETN65643.1     170
                                                XP_001846737.1     167
                                                    ABF18130.1     164
ATP synthase subunit G                              ACR54103.1     173
                                                    AAY66986.1     127
                                                XP_005182908.1     119
ATP synthase subunit O                              AGM32184.1     248
                                                XP_012220907.1     248
                                                   XP_968733.1     244
Krebs cycle
Citrate synthase                                    ETN60073.1     753
                                                    NP_999441.1    726
                                                    AAI66040.1     719
Aconitase                                           KMQ95155.1    1297
                                                    KZS13121.1    1266
                                                    CAB72317.1    1259
Succinyl-CoA synthetase                             ETN59000.1     455
subunit alpha
                                                XP_001868803.1     431
                                                    KDR08649.1     459
ADP-forming Succinyl-CoA                            BAN21224.1     595
ligase subunit beta
                                                    KDR17135.1     583
                                                   XP_970725.1     583
Mitochondrial NADP(+)-dependent                     KDR14081.1     687
Isocitrate dehydrogenase
                                                NP_001133196.1     642
                                                XP_007254547.1     644
Mitochondrial NAD(+)-Isocitrate                 XP_011425087.1     546
dehydrogenase subunit alpha
                                                    CEF67094.1     546
                                                XP_005092712.1     543
Mitochondrial NAD(+)-Isocitrate                 XP_005184353.1     467
dehydrogenase subunit beta
                                                 XPJH2546738.1     462
                                                XP_012234405.1     472
Mitochondrial NAD(+)-Isocitrate                 XP_008193347.1     479
dehydrogenase subunit gamma
                                                XP_008479949.1     474
                                                XP_011147544.1     446
Malate dehydrogenase                            NP_001188130.1     531
                                                   NP_998296.1     526
                                                    EFX69032.1     516
Fumarase                                           XP_967085.1     793
                                                    KDR21372.1     765
                                                   NP_957257.1     758
2-Oxoglutarate dehydrogenase                    XP_006566130.1    1510
                                                XP_012168263.1    1499
                                                XP_008193113.1    1505
Dihydrolipoyllysine-residue                     XP_001845679.1     511
succinyltransferase
                                                XP_012546089.1     494
                                                XP_005183707.1     501
Pyruvate dehydrogenase complex
Pyruvate dehydrogenase El                       XP_001017076.2     338
component subunit alpha
                                                    EJY81740.1     348
                                                    AAV32066.1     327
Pyruvate dehydrogenase El                           KDR20584.1     548
component subunit beta
                                                   NP_998319.1     503
                                                NP_001229442.1     532
Dihydrolipoyllysine-residue                     XP_011412451.1     171
acetyltransferase
                                                XP_013383918.1     181
                                                XP_013084075.1     177
Dihydrolipoyl dehydrogenase                        KDR 16622.1     781
                                                    AFP20522.1     776
                                                NP_001280524.1     770
Mitochondrial carriers, permeability
transition, and calcium transport proteins
Voltage-dependent anion channel                     ADJ94951.2     541
                                               XP_00184263 7.1     380
                                                    ETN58314.1     373
Adenine nucleotide                              XP_007557479.1     344
translocator isoform 3
                                                XP_008274460.1     339
                                               XP_008 324945.1     340
Cyclophilin D                                   XP_007551094.1     390
                                                XP_010746147.1     388
                                                NP_001002065.1     384
Phosphate carrier protein                       XP_013385882.1     488
                                                    KFM69008.1     488
                                                XP_011432203.1     499

Deduced protein name from                    Query cover (%)   % Ident
L. vannamei transcripts

Electron transport chain complex I
NADH dehydrogenase subunit F                     98                75
                                                 99                74
                                                 98                74
NADH dehydrogenase                               87                65
[ubiquinone] flavoprotein 2
                                                 89                61
                                                 85                53
NADH dehydrogenase                               18                57
[ubiquinone] flavoprotein 3
                                                 25                41
                                                 20                39
NADH dehydrogenase                               24                60
[ubiquinone] 1 beta subcomplex
subunit 4                                        26                46
                                                 25                38
NADH dehydrogenase                               44                31
[ubiquinone] 1 alpha subcomplex
subunit 5                                        44                33
                                                 44                32
NADH dehydrogenase                               69                32
[ubiquinone] 1 alpha subcomplex
subunit 6                                        66                33
                                                 67                33
NADH dehydrogenase                               56                80
[ubiquinone] iron-sulfur protein 7
                                                 58                74
                                                 53                78
NADH dehydrogenase                               52                66
[ubiquinone] 1 alpha subcomplex
subunit 8                                        52                61
                                                 52                57
NADH dehydrogenase                               90                44
[ubiquinone] 1 alpha subcomplex
subunit 9                                        88                34
                                                 82                37
NADH dehydrogenase                               30                47
[ubiquinone] 1 alpha subcomplex
subunit 11                                       30                46
                                                 27                41
NADH dehydrogenase                               98                44
[ubiquinone] 1 alpha subcomplex
subunit 12                                       98                42
                                                 99                45
Electron transport chain complex II
Succinate dehydrogenase subunit A                99                69
                                                 98                68
                                                 99                66
Succinate dehydrogenase subunit B                43                85
                                                 43                81
                                                 42                82
Electron transport chain
complex III
Cytochrome b5                                    85                45
                                                 85                44
                                                 88                41
Cytochrome b-cl complex subunit Rieske           50                75
                                                 58                67
                                                 58                63
Cytochrome b-cl complex subunit 1                79                38
                                                 79                38
                                                 74                37
Cytochrome b-cl complex subunit 2                61                41
                                                 61                43
                                                 56                42
Cytochrome b-cl complex subunit 7                38                61
                                                 38                61
                                                 38                59
Cytochrome cl                                    85                68
                                                 82                50
                                                 82                49
Electron transport chain
complex IV
Cytochrome c                                     26                90
                                                 26                82
                                                 26                86
COX 7 subunit A                                  38                36
                                                 21                48
                                                 21                49
COX 11                                           48                80
                                                 48                78
                                                 48                76
COX 15                                           46                70
                                                 46                68
                                                 46                62
COX 16                                           31                65
                                                 32                57
                                                 30                59
Electron transport
chain complex V
ATP synthase subunit D                           32                83
                                                 32                83
                                                 32                80
ATP synthase subunit E                           46                57
                                                 53                53
                                                 43                55
ATP synthase subunit F                           48                72
                                                 48                73
                                                 48                71
ATP synthase subunit G                           11                82
                                                 10                62
                                                 11                57
ATP synthase subunit O                           50                60
                                                 50                58
                                                 49                56
Krebs cycle
Citrate synthase                                 42                79
                                                 44                74
                                                 43                72
Aconitase                                        70                79
                                                 69                79
                                                 69                79
Succinyl-CoA synthetase                          57                78
subunit alpha
                                                 51                84
                                                 58                78
ADP-forming Succinyl-CoA                         69                68
ligase subunit beta
                                                 69                67
                                                 69                67
Mitochondrial NADP(+)-dependent                  52                78
Isocitrate dehydrogenase
                                                 55                70
                                                 54                72
Mitochondrial NAD(+)-Isocitrate                  67                73
dehydrogenase subunit alpha
                                                 67                75
                                                 64                75
Mitochondrial NAD(+)-Isocitrate                  12                66
dehydrogenase subunit beta
                                                 12                65
                                                 12                67
Mitochondrial NAD(+)-Isocitrate                  53                68
dehydrogenase subunit gamma
                                                 57                64
                                                 53                67
Malate dehydrogenase                             72                77
                                                 72                76
                                                 71                77
Fumarase                                         65                83
                                                 65                79
                                                 68                77
2-Oxoglutarate dehydrogenase                     85                76
                                                 85                76
                                                 89                72
Dihydrolipoyllysine-residue                      29                79
succinyltransferase
                                                 25                78
                                                 30                78
Pyruvate dehydrogenase complex
Pyruvate dehydrogenase El                        79                50
component subunit alpha
                                                 78                56
                                                 72                55
Pyruvate dehydrogenase El                        31                82
component subunit beta
                                                 32                75
                                                 32                79
Dihydrolipoyllysine-residue                      99                59
acetyltransferase
                                                 99                59
                                                 99                61
Dihydrolipoyl dehydrogenase                      60                75
                                                 60                75
                                                 60                74
Mitochondrial carriers, permeability
transition, and calcium transport proteins
Voltage-dependent anion channel                  38                94
                                                 38                63
                                                 38                61
Adenine nucleotide                               90                59
translocator isoform 3
                                                 92                58
                                                 91                59
Cyclophilin D                                    28                56
                                                 2S                53
                                                 2S                55
Phosphate carrier protein                        61                75
                                                 61                74
                                                 61                73

All sequences are encoded in the nuclear genome. The second column
contains the transcript or expressed sequence tags Genebank access
number previously reported for the protein analyzed in other species of
peneids.
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Article Details
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Author:Martinez-Cruz, Oliviert; Chimeo, Cindy; Rodriguez-Armenta, Chrystian M.; Muhlia-Almazan, Adriana
Publication:Journal of Shellfish Research
Article Type:Report
Date:Dec 1, 2017
Words:13085
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