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Evolution and functional diversity of aquaporins.

Abstract. In this review, we provide a brief synopsis of the evolution and functional diversity of the aquaporin gene superfamily in prokaryotic and eukaryotic organisms. Based upon the latest data, we discuss the expanding list of molecules shown to permeate the central pore of aquaporins, and the unexpected diversity of water channel genes in Archaea and Bacteria. We further provide new insight into the origin by horizontal gene transfer of plant glycerol-transporting aquaporins (NIPs), and the functional co-option and gene replacement of insect glycerol transporters. Finally, we discuss the origins of four major grades of aquaporins in Eukaryota, together with the increasing repertoires of aquaporins in vertebrates.

Introduction

Since the discovery of the archetypal molecular water channel (aquaporin-1, AQP1) in mammals towards the end of the twentieth century (Denker et al., 1988; Preston et al., 1992; Agre et al., 1993), increasing numbers of genome and transcriptome sequencing projects have resulted in the release of tens of thousands of orthologous channels in archaeal, bacterial, and eukaryotic organisms encompassing the three domains of life. Understanding how such gene diversity arose is challenging but necessary if we are to identify the historical events that led to the evolution of novel or constrained functions within or across taxonomic lineages.

The earliest evolutionary studies of diverse subfamilies of bacterial, plant, fungal, and animal aquaporins recognized two major phylogenetic divisions separating the water-selective type channels (Aqp) from the glycerol facilitators (Glp) (Park and Saier, 1996; Froger et al., 1998; Heymann and Engel, 1999). Such a phylogenetic dichotomy implied that an early gene duplication event led to the evolution of these two major functional forms in Prokaryota (Zardoya, 2005). Thus, until very recently, it was thought that Archaea have one aquaporin, termed AqpM, which permeates both water and glycerol (Kozono et al., 2003; Lee et al., 2005), while Bacteria have two, a water-selective channel, termed AqpZ (Calamita et al., 1995; Savage et al., 2003; Jiang et al., 2006), and a water-, urea-, and glycerol-transporting channel known as GlpF (Fu et al., 2000; Jensen et al., 2001). With the increasing troves of sequence data from different organisms, this view is changing. The latest studies are revealing an unexpected diversity of aquaporins in both prokaryotic and eukaryotic organisms (Bienert et al., 2013; Abascal et al., 2014; Finn et al., 2014; Verma et al., 2015). The aim of this review is to provide a brief summary of such diversity. It is not intended to give a comprehensive review of aquaporin structural biology and physiology, since these aspects have recently been reviewed elsewhere (Abascal et al., 2014; Ahmadpour et al., 2014; Bienert and Chaumont, 2014; Day et al., 2014; Ishibashi et al., 2014; Kaldenhoff et al., 2014; Li et al., 2014; Mukhopadhyay et al., 2014; Song et al., 2014; Tani and Fujiyoshi, 2014). Therefore, we present a short overview of the structure and function of aquaporins, and include a section on prokaryotic aquaporins to explain the origin by horizontal gene transfer (HGT) of some plant glycerol transporters. We review the origin and evolution of a new class of insect glycerol transporters, and finally we discuss the expansion of the eukaryotic superfamilies into four major grades of aquaporin and review recent advances in the origins of aquaporins in vertebrates. We use the term "grade" rather than "clade" to classify the different clusters of aquaporins in order to accommodate the similar but polyphyletic nature of the subfamilies.

Aquaporin Structure and Molecular Function

Aquaporins are integral membrane channels that primarily facilitate the passive transport of water and other small, uncharged solutes down their concentration gradients. Regardless of the permeability properties, however, the overall tertiary and quaternary structures of the core transmembrane domains (TMDs) are conserved. Four protomeric polypeptides form the individual water-conducting pores, which are folded in the endoplasmic reticulum and assembled primarily as homotetramers, but also occasionally as heterotetramers in membranebound vesicles of animals and plants (Verbavatz et al., 1993; Neely et al., 1999; Fetter et al., 2004; Pitonzo and Skach, 2005) (Fig. 1A). The prototypical protomer is thought to have evolved from an internal duplication and inversion of a trihelical-transmembrane segment causing the mature peptide to retain intracellular N- and C-termini of variable length and conformation (Pao et al., 1991). The integral membrane region is thus composed of six TMDs, three extracellular (A, C, E) and two intracellular (B, D) loops, and two inverted hemihelices on loops B and E that project opposing Asn-Pro-Ala (NPA) motifs to regulate the single-file conductance of water, while simultaneously functioning as a cation and a proton-excluding selectivity filter near the center of the molecule (Murata et al., 2000; Ho et al., 2009; Tani et al., 2009; Wree et al., 2011). A second constriction that contributes to proton exclusion is located in the outer channel vestibule and typically consists of aromatic residues and an arginine (ar/R) to form the major selectivity filter determining which molecular permeant can traverse the pore (Fu et al., 2000; Sui et al., 2001; Beitz et al., 2006a; Fu and Lu, 2007; Almasalmeh et al., 2014) (Fig. 1B). High-resolution crystallographic studies of fungal Aqy1, together with experimental studies of mammalian AQP1 and molecular dynamics simulations, have suggested that a synergistic effect between the NPA motifs and the ar/R selectivity filter breaks the connectivity of permeating water molecules to prevent proton transport via a Grotthuss mechanism, in which excess protons could shuttle through the hydrogen bond network of water, hydroxyl, and hydronium molecules (de Grotthuss, 1806; Wu etal., 2009; Li etal., 2011; Kosinska Eriksson et al., 2013). Based upon such findings, it has been suggested that the selectivity filter may have evolved as the major mechanism of proton exclusion, while the NPA motifs evolved to block cation transport through the pore (Li et al., 2011). In silico studies have further shown that the arrangement of the ar/R residues also correlates with the functional properties of the channel (Froger et al., 1998; de Groot and Grubmuller, 2005; Hub and de Groot, 2008; Oliva et al., 2010; Phongphanphanee et al., 2010; Lin et al., 2012; Zhang and Chen, 2013). For example, classical water-selective aquaporins such as eutherian AQP0, -1, -2, -4, or -5, which range in size from 28.1-34.8 kDa for the human channels, typically display a tight ar/R cluster in which His-201 on TMD5 of human AQP4 reduces the pore to about 1.5 Angstrom ([Angstrom]) and thus sterically

excludes the passage of glycerol (Ho et al., 2009). A three-dimensional reconstruction of the basal sarcopterygian coelacanth Aqp4 channel, based upon the structure mask of the crystallographically resolved human AQP4 ortholog (Protein Data Bank 3GD8), shows that this arrangement is evolutionarily conserved (Fig. 1C). Conversely, the eutherian water- and glycerol-transporting aquaporins (aquaglyceroporins, Glps) represented by AQP3, -7, -9, and -10, which range in size from 31.4-37.0 kDa for the human channels, have a more open structure due to a longer polypeptide region in loop E (Verma et al., 2015) and the tendency to display an uncharged constriction residue on TMD5. A model of the coelacanth Aqp3 channel based upon the structure mask of the bacterial glycerol uptake facilitator (GlpF) (Protein Data Bank 1LDF) illustrates that this more relaxed structure is also a conserved feature of Glps (Fig. 1D).

Although in silico structure-function studies can provide intuitive insight into the potential permeability properties of the various types of channels, their in vivo transport function may differ from such predictions due to differences in the primary structures, alternative splicing, posttranslational modifications, or the cellular environment in which they are expressed. For example, phosphorylation or dephosphorylation of N- or C-terminal residues, as well as in the intracellular or extracellular loops, is commonly associated with trafficking of vertebrate and plant aquaporins (Brown et al., 1998; van Balkom et al., 2002; Prak et al., 2008; Tingaud-Sequeira et al., 2008; Moeller et al., 2011; Tamma et al., 2011) , but can also result in gating (Tornroth-Horsefield et al., 2006; Nyblom et al., 2009; Verdoucq et al., 2014). The N-terminus is also associated with gating of fungal Aqyl (Fischer et al., 2009), while acidic pH and the [Ca.sup.2+] concentration in the cytoplasm is known to gate both plant plasma membrane intrinsic proteins (PIPs) (Tournaire-Roux et al., 2003; Alieva et al., 2006; Verdoucq et al., 2008; Frick et al., 2013) and vertebrate aquaporins (Zeuthen and Klaerke, 1999; Nemeth-Cahalan and Hall, 2000; Virkki et al., 2001; Nemeth-Cahalan et al., 2004; Chauvigne et al., 2015a). It is thus important to experimentally demonstrate the permeability properties of a given channel. The most direct evidence is obtained from homologous or heterologous expression experiments in amphibian oocytes, cultured cell lines, or yeast cells, or from reconstituted aquaporins in liposomes. Based upon such experiments, an overview of the major molecular solvents and solutes shown to permeate prokaryotic and eukaryotic aquaporins is presented in Table 1. The data for Eukaryota are organized into four grades: classical aquaporins, Aqp8-type aquaammoniaporins, unorthodox aquaporins, and Glps, according to the phylogenetic topology inferred from Bayesian inference of >700 non-redundant aquaporins (Fig. 1E).

The great majority of prokaryotic and eukaryotic aquaporin orthologs tested to date have been shown to transport water, indicating that this function was likely involved in cell volume regulation of the earliest life forms and has remained so in nearly all derived organisms. Some exceptions do, however, exist, including certain alleles of fungal Aqy2, which encode a premature stop codon in most laboratory strains (Laize et al., 2000; Carbrey et al., 2001). Plant type-1 PIPs (PIP1) and type-6 nodulin intrinsic proteins (NIP6) also display little or no water transport activity when expressed in amphibian oocytes (Chaumont et al., 2000; Dordas et al., 2000; Dixit et al., 2001; Bots et al., 2005; Temmei et al., 2005; Wallace et al., 2005; Secchi et al., 2007). Amongst animal aquaporins, Drosophila big brain (BIB), which lacks several amino acids upstream of the second NPA motif, lost the ability to transport water but evolved the dual capacity of a cation transporter and cellular adhesion molecule (Yanochko and Yool, 2002; Tatsumi et al., 2009). Other studies have suggested that the zebrafish Aqp0b ortholog of mammalian AQP0, which also functions as a cellular adhesion molecule (Costello et al., 1989; Gonen et al., 2004; Liu J., et al., 2011), is not a functional water transporter (Froger et al., 2010; Clemens et al., 2013). In this latter instance, however, a recent study of the pH sensitivies of tetraploid and diploid teleosts demonstrated that both zebrafish Aqp0a and -0b permeate water efficiently, but that an alternative allele exists (G19S) that abolishes the water transport function of Aqp0b (Chauvigne et al., 2015a). The first studies of unorthodox aquaporins Aqp11 and -12 indicated that these channels may not be functional at the plasma membrane due to their intracellular localization in vivo, a noncanonical NPC motif, and the replacement of the Arg residue in the ar/R selectivity filter by a Leucine (Leu) (Morishita et al., 2005; Gorelick et al., 2006). However, more recent studies have revealed, at least for mammalian AQP11, that both water and glycerol can permeate the pore (Yakata et al., 2007, 2011; Madeira et al., 2014).

In addition to the water transport function, Table 1 illustrates that a surprising diversity of molecules permeate different aquaporins, including small charged ions in selected channels such as mammalian AQP6 and insect BIB, or uncharged gases in several paralogs to large purines in mammalian AQP9, or disaccharides such as trehalose in certain mosquito aquaporins. While gas permeation is still debated (Kaldenhoff et al., 2014), observations that some channels that cluster on the water-selective branch of aquaporin trees naturally transport larger solutes such as glycerol and urea is beginning to blur the lines between the molecular function of a subfamily and its phylogenetic position. For example, rat AQP6. which is closely related to the water-selective AQP2 and -5 paralogs, is capable of transporting glycerol and urea under certain conditions (Holm et al., 2004). On a broader level, a novel class of aquaporins variously referred to as Rhodnius prolixus integral protein-like channels (RPIPs), Lygus hesperus integral protein-like channels (LHIPs), or AQP4/5 clade C channels (Drake et al., 2010, 2015; Wallace et al., 2012; Benoit et al., 2014a, b; Fabrick et al., 2014; Goto et al., 2015), have recently been classified as entomoglyceroporins (Eglp), since they specifically evolved to become the major glycerol transporters in insects (Finn et al., 2015). Experimental evidence has shown that the Eglp channels of both ancient and modern lineages of hexapod can transport a wide variety of polyols and urea (Kataoka et al., 2009a, b; Wallace et al., 2012; Drake et al., 2015; Finn et al., 2015). As shown in Figure IE, however, the Eglp channels are phylogenetically related to metazoan Aqp4 orthologs, which are classical water-selective channels. Nevertheless, experiments have demonstrated that the glycerol-transporting property of the Eglps specifically arose in basal hexapods in association with the substitution of the conserved TMD5 His in the ar/R selectivity filter of Aqp4-type channels to uncharged residues such as Ala and Ser in the Eglps (Finn et al., 2015). Remarkably, the Eglps subsequently replaced the ancestral Glps in the holometabolan insects, the most successful group of terrestrial organisms in the history of life, possibly due to the improved efficiency of Eglps for glycerol conductance (Finn et al., 2015) and an increased requirement for a colligative antifreeze (Duman, 2001; Stryer et al., 2010). The supplantation of Glps by Eglps thus may be viewed as an example of natural Darwinian selection at the molecular level.

Amongst other orthologs, mammalian AQP8- and the plant tonoplast intrinsic protein (TIP)-type channels, which have been termed aquaammoniaporins (Jahn et al., 2002), are not unique in transporting ammonia. Some classical aquaporins (AQP1, -6) and Glps from Protista to Mammalia also evolved this function. A separate semi-ubiquitous feature of aquaporins, regardless of their phylogenetic and structural characteristics, appears to be the conductance of hydrogen peroxide ([H.sub.2][O.sub.2]), which is commonly generated as a biproduct of mitochondrial oxidative phosphorylation in animals (Muller, 2000) or chloroplastic electron transport in plants (Ivanov et al., 2012). It has thus been suggested that most eukaryotic aquaporins likely evolved this capacity (Bienert and Chaumont, 2014) and are actively recruited to cell membranes to mediate cell signaling or to mitigate oxidative stress (Bienert et al., 2007; Dynowski et al., 2008; Almasalmeh et al., 2014; Bienert and Chaumont, 2014). Indeed, it was shown very recently that the rapid recruitment of a teleost Aqp8b channel to the inner mitochondrial membrane of the spermatozoon facilitates [H.sub.2][O.sub.2] efflux from the mitochondrial compartment, which is essential for the maintenance of the mitochondrial membrane potential, ATP production, and flagellar motility (Chauvigne et al., 2013, 2015b).

These examples thus hint at a broader spectrum of permeants for the aquaporin superfamilies of eukaryotic organisms, and it seems likely that this range will increase as ever more exotic properties of channels are discovered. It will be important, however, to place such novel functions in a phylogenetic framework in order to refine our understanding of how the aquaporin superfamily evolved its functional diversity in different organisms. This is particularly true if a given lineage of organisms loses a branch of aquaporins involved in basic biochemical pathways. For example, the available evidence now indicates that the glp genes associated with glycerol transport were independently lost in the megadiverse holometabolan insects and higher plants (Zardoya et al., 2002; Abascal et al., 2014; Finn et al., 2015), yet both lineages acquired new glycerol transporters from unexpected quarters. The next section explains how plants likely acquired a new set of glycerol transporter genes from bacteria.

Aquaporin Evolution from Prokaryota to Eukaryota

It has been suggested that half of all eukaryotic genes have their origins in Prokaryota (Lodgson, 2010). With the identification and phylogenetic analysis of the first prokaryotic aquaporins, it became clear that the eukaryotic aquaporin superfamily was also rooted within the archaeal and bacterial domains (Pao et al., 1991; Park and Saier, 1996). However, the flow of genes from prokaryotes to eukaryotes has taken two routes. The semivertical hybrid route may have occurred as a result of symbiosis shortly before the great oxygen crisis about 2.5 Ga (Gu, 1997) (McInerney et al., 2014), while the second occurred at different time periods via HGT (Andersson, 2005; Keeling and Palmer, 2008). It is not yet possible to assess the full dimensions of aquaporin evolution via HGT in Eukaryota due to the current paucity of data in non-metazoan organisms. Amongst plants, however, it has been reported that glycerol transporters in the form of Nodulin 26-like integral proteins (NIPs, Fortin et al., 1987; Rivers et al., 1997; Dean et al., 1999) evolved from bacterial AqpZ via HGT and functional recruitment (Zardoya et al., 2002). While this view has been maintained in the contemporary literature, where it is suggested that the first residue of the ar/R filter mutated to tryptophan (Trp), and the P1 and P5 sites were, respectively, replaced by aromatic and small hydrophobic amino acids to acquire glycerol transport capacity (Wallace et al., 2002; Abascal et al., 2014), recently available data hint at a different scenario (Finn et al., 2014). Based upon the molecular phylogeny of prokaryotic aquaporins, it has generally been assumed that bacterial genomes encode Aqps and Glps (Zardoya, 2005; Danielson and Johanson, 2010; Bienert et al., 2013; Abascal et al., 2014). However, a separate molecular phylogenetic analysis based upon Bayesian inference revealed a more complex evolution of prokaryotic aquaporins, in which four grades (AqpZ, AqpN, AqpM, and GlpF) were resolved with high statistical inference (Finn et al., 2014). In some Firmicutes, such as members of the order Bacillales, the newly identified AqpN grade coexists with AqpZ and GlpF. These new findings likely reflect the increased availability of genome sequences in public databases, which were not fully analyzed in earlier studies. Indeed, a more recent analysis using maximum parsimony and neighbor-joining protocols also found four distinct clusters of channels in Archaea, but only two in Bacteria (Verma et al., 2015). Although future studies will need to validate these findings, the surprising observation in one of the studies is that both archaeal and bacterial aquaporins are represented in each of the four grades (Finn et al., 2014), which is potentially consistent with the notion of a ring of life at the bottom of the tree of life (Rivera and Lake, 2004).

An interesting feature of the prokaryotic aquaporins clustering within the AqpN grade is that it contains species associated with nitrite oxidation in soil, which have only a 34% amino acid identity to the major intrinsic protein of nitrogen-fixing Rhizobium species found in the symbiosomes of root nodules of leguminous plants (Clarke et al., 2014). We therefore re-evaluated the HGT hypothesis of plant NIPs in light of these new data, using Bayesian inference (Fig. 2A). These analyses, conducted for the first time, here provide robust statistical support for proposing that the origin of plant NIPs arose via HGT from bacterial AqpN rather than AqpZ, with the last common ancestor closely related to nitrite-oxidizing members of the Chloroflexi phylum. Inspection of the ar/R residues and the P1-P5 sites thought to delineate the selectivity of water and glycerol-transporting channels (Froger et al., 1998) reveals that there was not a major functional shift in either the ar/R or the P1-P5 sites (Fig. 2B, C) during this transition. Consequently, our data suggest that the glycerol-transporting function was already established in the AqpN channels prior to the HGT event. Since NIPs are also considered essential for metalloid transport in plants (Pommerrenig et al., 2015), it would be interesting to establish whether metalloid transport was an ancestral biophysical feature of AqpN-type channels. While further experiments will need to verify this theory, it is nevertheless clear that following the HGT event, NIPs have significantly expanded in plant genomes due to serial rounds of tandem and genome duplications (Quigley et al., 2001; Liu et al., 2009). At least five nip genes are present in the moss (Physcomitrella patens) genome (Danielson and Johanson, 2008) and four in the genome of maize (Zea mays) (Chaumont et al., 2001), while eight to thirteen have been reported in the genomes of Arabidopsis thaliana, rice (Oryza sativa), grapevine (Vitis viniferd), black cottonwood tree (Populus trichocarpa), upland cotton (Gossypium hirsutum), tomato (Solanum lycopersicum), potato (Solanum tuberosum), soybean (Glycine max), and cabbage (Brassica oleracea) (Johanson et al., 2001; Quigley et al., 2001; Sakurai et al., 2005; Fouquet et al., 2008; Gupta and Sankararamakrishnan, 2009; Park et al., 2010; Reuscher et al., 2013; Venkatesh et al., 2013; Zhang et al., 2013; Diehn et al., 2015). The differences in the numbers of paralogs are thought to be associated with tandem duplication and the degree of polyploidy (Quigley et al., 2001; Park et al., 2010; Zhang et al., 2013), which is widespread amongst the majority (>70%) of flowering plants (angiosperms) (Blanc and Wolfe, 2004; Adams and Wendel, 2005; Meyers and Levin, 2006; Otto, 2007).

Aquaporin Diversity in Eukaryota

Despite the vast array of extant eukaryotic species, it has been suggested that all of these organisms can be grouped within two superclades, the Bikonta and Unikonta (Cavalier-Smith, 2002; Minge et al., 2009). In turn, these superclades are thought to comprise six major supergroups or kingdoms of eukaryotic life: Excavata, Rhizaria, Chromalveolata, Plantae, Amoebozoa, and Opisthokonta, wherein the latter contains Fungi and Animalia (Cavalier-Smith, 2002; Stechmann and Cavalier-Smith, 2002). In the present context, Figure 1E encapsulates some of this diversity in the form of aquaporins for Unikonta. Based upon an examination of available eukaryotic genomes, Figure 3 provides a schematic summary of the grades and prevalence of aquaporin paralogs found in Eukaryota. Absent from this scheme are members of the Rhizaria; however, BLAST searches of the Bigelowiella natans genome, which is a mixotrophic chlorarachniophyte alga, indicates that at least two paralogs are present in this organism. Consequently, it is likely that Aqps and Glps are encoded in the genomes of representative organisms from all kingdoms of life. Within Chromalveolata and Excavata, however, it is nevertheless apparent that some unicellular members of the Stramenopiles, such as Phytophthora infestans, have rapidly expanded the Glp branch at the expense of Aqps, while members of the Alveolata such as Paramecium tetraurelia and Euglenozoa, including Trypanosoma cruzi, expanded the Aqp branch at the expense of Glps (Abascal et al., 2014). Consequently, the concept of simplification from multicellular to unicellular organisms does not hold for the aquaporin superfamily. Indeed, the genome of the free-living P. tetraurelia encodes more paralogs than any tetrapod, possibly highlighting the physical challenges of exposure to changing environments (von Bulow and Beitz, 2015).

Available data suggest that the first major diversification of aquaporins occurred in land plants (Embryophyta), with seven classes or subfamilies currently documented for non-vascular plants (Bryophyta) such as moss (Danielson and Johanson, 2008). This includes the PIPs, hybrid intrinsic proteins (HIPs), X intrinsic proteins (XIPs), TIPs, NIPs, GlpF-like intrinsic protein (GIP), and small basic intrinsic proteins (SIPs). Between four and five of the bryophyte classes of aquaporin are found in angiosperms, and it has been proposed that the GIP and HIP classes were lost in paired leaf seed plants (Dicotyledonae), while the XIP class was further lost in single seed leaf plants (Monocotyledonae) (Danielson and Johanson, 2008). More recent data for the aquaporin superfamily of one of the oldest living lineages of vascular land plants (Lycophyta), the spike moss (Selaginella moellendorffii), indicate that the GIP subfamily may have been lost prior to the evolution of Lycophyta (Anderberg et al., 2012), while recent data for angiosperms support the absence of the HIP subfamily in Dicotyledonae (Gupta and Sankararamakrishnan, 2009; Park et al., 2010; Reuscher et al., 2013; Venkatesh et al., 2013; Zhang et al., 2013; Diehn et al., 2015). Further comprehensive studies of ferns (Sessa et al., 2014) and basal seed plants such as conifers (Gymnospermae), e.g., the Norway spruce (Nystedt et al., 2013), need to be conducted to determine whether the loss of the HIP subfamily occurred prior to the evolution of ferns, gymnosperms, or angiosperms. Amongst angiosperms, however, the number of paralogs varies between 33 and 71, with the highest gene copy number currently found in the allotetraploid upland cotton (Park et al., 2010).

Phylogenetic reconstructions of the aquaporin superfamilies in Plantae in relation to those present in Animalia have consistently clustered plant PIPs with animal Aqp4 orthologs and plant TIPs with animal Aqp8 orthologs (Zardoya and Villalba, 2001; Zardoya, 2005; Gomes et al., 2009; Soto et al., 2012; Abascal et al., 2014). Some of these studies further indicated that HIPs and XIPs may also repesent orthologs of animal Aqp8 channels, while SIPs are unorthodox aquaporins related to the Aqp 12-like genes of Metazoa (Gomes et al., 2009; Abascal et al., 2014). Although vascular plants lack true Glps, the acquistion of NIPs and GIPs have compensated for this function (Zardoya et al., 2002; Abascal et al., 2014). Amongst basal Metazoa, including sponges (Porifera), corals, and sea anemones (Cnidaria), the origins of four major grades of aquaporins present in deuterostome organisms have been resolved via Bayesian inference (Finn et al., 2014). These combined data sets therefore suggest that the aquaporin superfamilies of eukaryotic organisms can be segregated into four major grades, as shown in Figure 3. We have recently conducted extensive analyses of aquaporins encoded in arthropod genomes (Finn et al., 2015; Stavang et al., 2015), and we have further screened the genomes of members of the Lophotrochozoa to provide a preliminary assessment of the diversity of aquaporins present in Protostomia. We have not found any ortholog that did not fall within the four-grade classification depicted in Figure 3. Considering that lineage-specific gene losses are thought to account for the differences in gene repertoires of eukaryotic genomes, particularly in fungi, nematodes, and insects (Krylov et al., 2003), each of which also lacks at least one of the major grades of aquaporin, while others, including plants, molluscs, worms, and all deuterstome animals retain all four, it is plausible that the four grades of aquaporin arose deep within the eukaryotic lineage (Perez Di Giorgio et al., 2014). While such grades may also have arisen as a result of convergent evolution, it is certainly clear that different grades of aquaporins were differentially expanded and lost in the separate lineages, including the well-studied mammals.

Origin of Aquaporins in Vertebrates

Until recently, the mammalian complement of aquaporins was thought to consist of up to thirteen classes or subfamilies (AQP0 to -12) (King et al., 2004; Kruse et al., 2006; Gomes et al., 2009; Ishibashi et al., 2009). However, new studies have shown that older lineages of mammals (Metatheria and Prototheria) retain additional classes (AQP13 and -14) (Finn and Cerda, 2011; Finn et al., 2014). Yet more subfamilies (Aqp15 and -16) have been identified in non-mammalian vertebrates, including lampreys (Hyperoartia), sharks (Chondrichthyes), ray-finned fishes (Actinopterygii), coelacanths (Actinistia), frogs (Amphibia), alligators (Crocodylia), and turtles (Testudines) (Finn et al., 2014). Two of the new subfamilies, Aqp14 and -15, are classical aquaporins related to Aqp4 and Aqp1, respectively (Fig. 4), while Aqp13 is a Glp expressed in the oocytes of frogs (Virkki et al., 2002), and Aqp16 is closely related to the Aqp8-type of aquaammoniaporins. The permeability properties of Aqp14-, -15-, and -16-type channels have yet to be tested.

The number of subfamilies does not always reflect the number of paralogs in a given organism. With the exception of gorillas and humans, which harbor duplicates of AQP12, and excluding the AQP7 and -10 pseudogenes in humans and mice, respectively (Morinaga et al., 2002; Finn et al., 2014), the mammalian complement of aquaporins precisely reflects the number of subfamilies. The paralog counts of sauropsids also generally reflect the different subfamilies, although lizards (Iguania) and snakes (Serpentes) encode additional AQP5-like genes. The numerical relationship between paralogs and subfamiles is more divergent in Amphibia due to multiple copies of AQP6 (AQP6ub, AQP6vs1, AQP6vs2), which are, respectively, expressed in the urinary bladder and ventral skin (Suzuki et al., 2007; Suzuki and Tanaka, 2009; Suzuki et al., 2015), two copies of AQP5, representing a canonical channel and an AQP5-like gene, and three copies of AQP4 (Finn et al., 2014; Suzuki et al., 2015). In contrast to the Tetrapoda, the genomes of bony fishes (Teleostei) typically encode twice the number of paralogs (20-26) compared to the retained number of subfamilies (11-12), while the holostean spotted gar (Lepisosteas oculatus) has 13 paralogs spread amongst 11 subfamilies. The data for teleost aquaporins are thus consistent with a tertiary round of whole genome duplication (WGD) after the lineage separated from Holostei (Amores et al., 2011). Many of the teleost aquaporins show redundant expression in tissues, which could suggest subfunctionalization, but in most cases their physiological roles remain to be established (Cerda and Finn, 2010).

Paleopolyploidy events cannot explain the origin of all of the piscine paralogs, however. Several gene copies arose via tandem duplication, including aqp1aa, -1ab1, -1ab2, aqp3aa, -3ab, aqp8aa, -8ab, and aqp10aa, -10ab (Tingaud-Sequeira et al., 2008, 2010; Cerda and Finn, 2010; Zapater et al., 2011; Finn and Cerda, 2011; Finn et al., 2014). Although some of these paralogs tandemly duplicated within the teleost lineage, others including aqp3, -3L, -8aa, -8ab, -10, and -10L duplicated earlier in Chondrichthyes or prior to the separation of Holostei from Teleostei (Finn et al., 2014). Consequently, due to the combination of tandem duplication and WGD, the highest aquaporin gene copy number in any vertebrate is currently found in the tetraploid Atlantic salmon (Salmo salar), with 42 paralogs (Finn et al., 2014; Stavang et al., 2015), consistent with a fourth round of WGD in Salmonidae some 88-103 Ma (Berthelot et al., 2014; Macqueen and Johnston, 2014).

Since the first suggestions that vertebrate genomes were shaped by serial paleoploidy events (Ohno et al., 1968; Ohno, 1970), an expanding volume of studies has examined the evolutionary consequences of gene duplication (reviewed by Innan and Kondrashov, 2010; Kondrashov, 2012; Canestro et al., 2013). Although three rounds of WGD are recognized (Meyer and Schartl, 1999; Donoghue and Purnell, 2005; Finn and Kristoffersen, 2007; Braasch et al., 2008; Van de Peer et al., 2009), the timing of the second round near the base of vertebrate evolution remains uncertain (Kuraku et al., 2009). With respect to the aquaporin superfamily, seven classes (aqp01, -3L, -4, -8, -10L, -12, and -14) have been identified in the genomes of lampreys (Hyperoartia), which are extant representatives of jawless vertebrates (Agnatha). More than twice that number (17, aqp0 to -16) have been identified in the genomes of different jawed vertebrates (Gnathostomata) (Finn et al., 2014). Thus, for the aquaporin superfamily the occurrence of a second round of WGD after the separation of Gnathostomata from Agnatha would provide a parsimonious explanation for the divergent numbers of subfamiles in these lineages. This timing is further supported by observations of karyotype expansion between Cyclostomata and Gnathostomata (Nakatani et al., 2007) and earlier reconstructions of other gene families, including homeobox (Neidert et al., 2001; Force et al., 2002; Tank et al., 2009), pigmentation genes (Braasch et al., 2008), vitellogenin (Finn and Kristoffersen, 2007; Babin, 2009; Finn et ai, 2009; Kristoffersen et al., 2009), chemosensory receptors (Libants et al., 2009), adenohypophyseal hormones (Kawauchi and Sower, 2006; Sower et al., 2008), and thyroid and glycoprotein hormone receptors (Freamat and Sower, 2008; Chauvigne et al., 2010; Applebaum et al., 2012).

Interestingly, at least one set of the lamprey genes (aqp 10L1 and -10L2) appears to have arisen via tandem duplication, while another may have arisen as two separate genes (aqp0 and -1) that subsequently fused (aqp01) (Finn et al., 2014). Although further studies will need to examine whether an aqp0-like ortholog exists in hagfishes (Hyperotreti), the expression of the aqp01 gene in the eye of the sea lamprey (Petromyzoti marinus) is consistent with the evolution of multifocal lenses in Hyperoartia after the lineage diverged from Hyperotreti (Gustafsson et al., 2008). The subsequent evolution of aqp0 channels in Gnathostomata suggests that this multi-functional class of aquaporin experienced purifying selection. In all members of the Gnathostomata except birds (Aves), the aqp0 genes encode 263 amino acids with less than 32% of the residues substituted among Chondrichthyes, Actinopterygii, Actinistia, and Tetrapoda. This represents a divergence time spanning over 500 million years (Hedges, 2009). Similarly, a recent analysis of four aqp0 genes in the Atlantic salmon revealed that the salmonid-specific genomic duplicates have only diverged by 4%-6% at the amino acid and nucleotide levels, respectively, over about 100 million years (Chauvigne et al., 2015a). Such a slow rate of substitution (0.04 amino acids/million years) starkly contrasts with the aqp1ab genes of Teleostei, which have experienced up to 81% amino acid substitution during the same evolutionary time period (Zapater et al., 2011). These data highlight the purifying selection of the aqp0 genes that are essential for vision (Verkman, 2003; Froger et al., 2010; Schey et al., 2014).

A salient feature of the approximately 55,000 extant vertebrates is that roughly half now inhabit terrestrial environments (Tetrapoda), while the other half have remained in aquatic environments (fishes). Recent studies of 29 actinopterygian and 90 sarcopterygian genomes revealed that the AQP2, -5, or -6 gene clusters represent a genomic apomorphy since they are only found in the lobe-finned fish lineage (Sarcopterygii), including tetrapods that secondarily adapted to the aquatic environment (Cerda and Finn, 2010; Tingaud-Sequeira et al., 2010; Finn and Cerda, 2011; Xu et al., 2013; Finn et al., 2014). The oldest orthologs of AQP2, -5, and -6 are currently found in the coelacanth (Latimeria chalumnae) with three aqp2-like paralogs (aqp2a, -2b, and -2c, Fig. 4) that are syntenic to the tetrapod AQP2, -5, and -6 gene clusters. Similar aqp2-like genes that are reported as paralogs of AQPO (Aqp0p) have also been identifed in lungfishes (Dipnoi) (Konno et al. 2010). While the function of the coelacanth Aqp2-like channels remains unknown, the physiological role of the Aqp2-like channels in lungfishes is to promote antidiuresis during terrestrial estivation in a manner entirely synonymous with the arginine-vasoticin-induced regulation of AQP2 channels in the kidneys of modern tetrapods (Konno et al., 2010). Given the critical water-conserving roles that the AQP2, -5, and -6 channels play in the skin, urinary bladder, salt glands, and kidneys of extant amphibians, sauropsids, and mammals (Nishimura and Fan, 2002; Muller et al., 2006; Suzuki et al., 2007; Boone and Deen, 2008; Nishimura, 2008; Lau et al., 2009; Suzuki and Tanaka, 2009; Suzuki et al., 2015), it seems likely that their lineage-specific evolution was permissive for tetrapod terrestrial adaptation (Finn et al., 2014). This would be the case regardless of the mechanism of gene duplication, i.e., WGD or tandem duplication, which might be inferred from their linkage to aqp0 genes in the chromosomes of many vertebrates. The identification of an aqp2-like ortholog in the ancient chondrichthyan lineage would resolve the origin of the apomorphic gene clusters in vertebrates.

Conclusions

The available data indicate that multiple forms of aquaporins are found in virtually all organisms, including every eukaryotic kingdom of life. The diversity of molecules that permeate different channels is beginning to blur the lines between the molecular function of a subfamily and its phylogenetic position. The recent discovery of the insect Eglps, which are phylogenetically related to classical, water-selective Aqp4 channels, but which evolved to become the major glycerol transporters in holometabolan insects, clearly illustrates this point. While some microbes may lack aquaporins, other single-celled organisms can harbor higher gene copy numbers than modern mammals. An unexpected diversity of aquaporins is found in Archaea and Bacteria, with four intermixed grades (AqpZ, AqpN, AqpM, and GlpF) established in these domains of life. The first major diversification of aquaporins in Eukaryota is observed in land plants, with up to seven major classes established in the oldest bryophyte lineages (PIP, HIP, XIP, TIP, NIP, GIP, and SIP). The loss of Glps in the embryophytic land plants was compensated for by the acquisition by horizontal gene transfer of the NIP class of glycerol transporter. New data analyzed here suggest that the NIP genes originated from the AqpN class of aquaporins of nitrite-oxidizing Bacteria, and that there was no functional recruitment of residues to confer the glycerol-transporting property. The aquaporin repertoires of other multicellular eukaryotes are found to cluster within four major grades (Aqp4-like, Aqp8-like, Aqpl 2-like, and Glp), supporting the notion that a major divesification of these genes could have occurred deep in the evolution of Eukaryota. Not all lineages retain paralogs from each of the aquaporin grades, however, with current data indicating that Nematoda lack Aqp4-like orthologs and Arthropoda lack Aqp8-like orthologs. Nevertheless, the data show that the aquaporin grades independently expanded by gene duplication in the different lineages. While recurrent WGD and tandem duplications are sufficient to explain the origin of the majority of eukaryotic aquaporins, at least one gene was found to have fused in lampreys. Although the aquaporin repertoires have thus increased in vertebrates, with novel forms retained in non-eutherian members (Aqpl3, -14, -15, and -16), the expansion was unequal, with unique gene clusters of AQP2, -5, and -6-related paralogs only evolving in the sarcopterygian lineage. Owing to the vital, water-conserving roles of the AQP2, -5, and -6 gene clusters in extant amphibians, sauropsids, and mammals, it is suggested that lineage-specific evolution of these apomorphic gene clusters was permissive for vertebrate terrestrial adaptation.

Acknowledgments

This work was supported by the Research Council of Norway (RCN) projects 204813/F20 and 224816/E40 to R.N.F., and the Spanish Ministry of Economy and Competitiveness (MINECO), project AGL2013-41196-R to JC.

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RODERICK NIGEL FINN (1,2,*) AND JOAN CERDA (3)

(1) Department of Biology, Bergen High Technology Centre, University of Bergen, Norway; (2) Institute of Marine Research, Nordnes, 5817 Bergen, Norway; and (3)Institut de Recerca i Tecnologia Agroalimentaries (IRTA)-Institut de Ciencies del Mar, Consejo Superior de Investigaciones Cientificas (CSIC), 08003 Barcelona, Spain

(*) To whom correspondence should be addressed. E-mail: nigel.finn@uib.no

Abbreviations: AQP, aquaporin; ar/R, aromatic-arginine selectivity filter; Arg, arginine; ATP, adenosine triphosphate; BIB, big brain; Eglp, entomoglyceroporin; Ga, billions of years ago; GIP, GlpF-like intrinsic protein; Glp, aquaglyceroporin; HGT, horizontal gene transfer; HIP, hybrid intrinsic protein; His, histidine; Leu, leucine; LHIP, Lygus hesperus integral protein-like channel; NIP, plant nodulin 26-like integral protein; NPA, asparagine-proline-alanine; NPC, asparagine-proline-cysteine; PIP, plasma membrane intrinsic protein; RPIP, Rhodnius prolixus integral protein-like channel; SIP, small basic intrinsic protein; TIP, plant tonoplast intrinsic protein; TMD, transmembrane domain; Trp, tryptophan; XIP, X intrinsic protein; WGD, whole genome duplication.

Table 1
Major solvents and solutes shown to permeate through archaeal,
bacterial, plant, insect, and vertebrate aquaporins

Aquaporin
grade         Ortholog        Permeant

Classical     AQP0            Water, C[O.sub.2]
aquaporins
              AQP1            Water, C[O.sub.2], NO, [H.sub.2][O.sub.2],
                              N[H.sub.3]









              AQP2            Water

              AQP4            Water, C[O.sub.2]

              AQP5            Water. C[O.sub.2]


              AQP6            Water, glycerol, urea, anions,
                              N[O.sub.3.sup.-], C[O.sub.2], N[H.sub.3]
              PRIP            Water, urea


              BIB             Cations
              DRIP            Water


              Eglp            Water, glycerol, polyols, trehalose



              PIP             Water

Aqp8-related  AQP8            Water, glycerol, urea, N[H.sub.3],
                              [H.sub.2][O.sub.2]


                                 Geyer et al., 2013
              Nematode Aqp8L  Water
              TIP             Water, glycerol, [H.sub.2][O.sub.2],
                              N[H.sub.3],

              XIP             Glycerol, urea, boric acid
              HIP             Unknown
              NIP             Water, glycerol, formamide,
                              arsenite, boric acid, silicic acid,
                              N[H.sub.3],


              Aqyl, Aqy2      Water
                                 Madeira et al., 2014
Unorthodox    AQP 11          Water, glycerol
 aquaporins
Bacteria      AqpZ            Water
Glps          AQP3            Water, glycerol, urea, antimonite,
                              arsenite, polyols



              AQP7            Water, glycerol, urea, antimonite,
                              arsenite, N[H.sub.3],

              AQP9            Water, glycerol, urea, carbamides,
                              polyols, purines, pyrimidines,
                              antimonite, arsenite, C[O.sub.2],
                              N[H.sub.3],

              AQP 10          Water, glycerol, urea; antimonite,
                              arsenite
                                 et al., 2010
              AQP 13          Water, glycerol, urea
              Nematode Glp    Water, glycerol
              Plasmodium Glp  Water, glycerol, N[H.sup.3],
              Fps1            Water, glycerol, methylamine, N[H.sub.3],
                              antimonite, arsenite, boric acid

Bacteria      GlpF            Water, glycerol, urea, antimonite,
                              arsenite, polyols, lactate
Archaea       AqpM            Water, glycerol



Aquaporin
grade           References

Classical       Mulders et al., 1995; Virkki et al., 2001;
aquaporins      Froger et al., 2010; Clemens et al.,
                2013; Geyer et al., 2013;
                Chauvigne et al., 2015b
                Preston et al., 1992; Yang and Verkman,
                1997; Nakhoul et al., 1998; Nakhoul et
                al., 2001; Fabra et al., 2006; Herrera et
                al., 2006; Musa-Aziz et al., 2009; Raldua
                et al., 2008; Tingaud-Sequeira et al.,
                2008, 2009, 2010; Chen et al., 2010;
                Zapater et al., 2011; Itel et al., 2012;
                Geyer et al., 2013; Almasalmeh et al.,
                2014; Martos-Sitcha et al., 2015
                Fushimi et al., 1993; Deen et al., 1994;
                Bai et al., 1996; Yang and Verkman, 1997
                Jung et al., 1994; Yang and Verkman, 1997;
                Musa-Aziz et al., 2009; Geyer et al., 2013
                Raina et al., 1995: Yang and Verkman,
                1997; Musa-Aziz et al., 2009; Geyer et
                 al., 2013
                Yasui et al., 1999; Ikeda et al., 2002;
                Holm et al., 2004; Geyer et al., 2013
                Kikawada et al., 2008; Liu K., et al.,
                2011; Herraiz et al., 2011; Goto et al.,
                 2011; Philip et al., 2011
                Yanochko and Yool, 2002
                Le Caherec et al., 1996; Kaufmann et al.,
                2005; Shakesby et al., 2009; Nagae et al.,
                2013
                Kikawada et al., 2008; Kataoka et al.,
                2009a, b; Wallace et al., 2012; Fabrick
                et al., 2014; Drake et al., 2015;
                Finn et al., 2015
                Tournaire-Roux et al., 2003; Schuurmans
                et al., 2003; Bellati et al., 2010
Aqp8-related    Ishibashi et al., 1997b; Jahn et al.,
                2004; Tingaud-Sequeira et al., 2010;
                Engelund et al., 2013; Chauvigne et al.,
                2013; Chauvigne et al., 2015a

                Huang et al., 2007
                Maurel et al., 1993; Jahn et al., 2004;
                Holm et al., 2005; Bienert et al., 2007;
                Li et al., 2008
                Bienert et al., 2011

                Dean et al., 1999; Niemietz and Tyerman,
                2000; Schuurmans et al., 2003; Wallace and
                Roberts. 2005; Ma et al., 2006; Bienert
                et al, 2008; Mitani et al., 2008; Takano
                et al., 2008; Hwang et al., 2010
                Laize et al., 1999; Carbrey et al., 2001;

Unorthodox      Ikeda et al., 2011; Yakata et al., 2011
 aquaporins
Bacteria        Calamita et al., 1995
Glps            Echevarria et al., 1994; Ishibashi et al.,
                1994; Ma et al., 1994; Yang and Verkman,
                1997; Hamdi et al., 2009; MacIver et al.,
                2009; Tingaud-Sequeira et al., 2009, 2010;
                Chauvigne et al., 2011
                Ishibashi et al., 1997a; Liu et al., 2002;
                Tingaud-Sequeira et al., 2010; Chauvigne
                et al., 2013; Geyer et al., 2013
                Ishibashi et al., 1998; Tsukaguchi et al.,
                1999; Liu et al., 2002; Carbrey et al.,
                2003; Hamdi et al., 2009; Tingaud-Sequeira
                et al., 2010; Chauvigne et al., 2013;
                Geyer et al., 2013
                Ishibashi et al., 2002; Santos et al.,
                2004; Hamdi et al., 2009; Tingaud-Sequeira

                Virkki et al., 2002
                Huang et al., 2007
                Zeuthen et al., 2006
                Luyten et al., 1995; Sutherland et al.,
                1997; Wysocki et al., 2001; Beitz
                et al., 2006b; Nozawa et al., 2006
Bacteria        Maurel et al., 1994; Calamita et al.,
                1995; Sanders et al., 1997; Meng et al.,
Archaea         2004; Bienert et al., 2013
                Kozono et al., 2003   0

Although the major permeants are indicated, there may be additional
permeants not listed here that are transported by specific aquaporins
in different organisms.
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