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Syntrophic Propionate Degradation in Anaerobic Digestion: A Review.



Degradation of propionate is a central issue for improving performance of an anaerobic digestion system, because propionate is an intermediate product, which is generally accumulated in anaerobic digesters. Many factors containing pH, temperature, volatile fatty acids, hydrogen partial pressure, and toxins would inhibit the biodegradation of propionate under anaerobic conditions. Propionate can be oxidized only if a syntrophic association is carried out by propionate-oxidizing bacteria and hydrogen-consumming bacteria. As propionate degraders, syntrophic propionate-oxidizing bacteria (SPOB) play an important role in anaerobic food chain and anaerobic global carbon cycles. However, these microorganisms are often difficult to be isolated and cultured as result of extremely fastidious metabolism type. To date, only ten species were identified as SPOB, which belonged to class Deltaproteobacteria or Firmicutes.

Most identified SPOB degrade propionate through methylmalonyl coenzyme A pathway (MMC) pathway and genomic information indicated the catabolic pathways are controlled by ecological factors and/or global cellular conditions. Further investigation is needed on the response mechanism of SPOB to the environmental factors. To prevent anaerobic digestor from propionate accumulation, it is important to detect SPOB in time and forecast the accumulation of propionate with mathematical models. (c) 2012 Friends Science Publishers

Key Words: Anaerobic digestion; Propionate degradation; Syntrophic propionate-oxidizing bacteria; Ecophysiology; Phylogeny


Anaerobic digestion technology was paid attention by more researchers, because of the removal of organic pollutants in solid waste and wastewater and simultaneously produces methane as an energy resource (Wang et al., 2004; Mahmood et al., 2011). It is complex with a number of sequential and parallel steps that are carried out by mainly four groups of microorganisms including primary fermenting bacteria, syntrophic acetogens, homoacetogens and methanogenic archaea (Kosaka et al., 2006; Jha et al.,2011). Each group of microbes have specific metabolic functions (Fig. 1). Propionate is an important intermediate during anaerobic digestion of organic polymers.

Its degradation into acetate and H2/CO2 (and then to CH4) accounts for 6% ~ 35% in the total methanogenesis (Glissmann and Conrad, 2000). However, the oxidation of propionate is energetically unfavorable with a standard change in Gibbs free energy (DGdeg') of +76 kJ per mol reaction as illustrated in Table I (MUller et al., 2010). Thermodynamically, propionate is more difficult to be anaerobically oxidized than butyrate, lactate and ethanol. So, it is usually accumulated in an anaerobic digester, even resulting in failure of the anaerobic digestion process (Kaspar and Wuhrmann, 1978; Van Lier et al., 1996; Shah et al., 2009; Ghasimi et al., 2009; Liu et al., 2010). Anaerobic oxidation of propionate is affected by many factors, including pH, temperature, hydrogen partial pressure, volatile fatty acids (VFAs), reactor configuration and organic compounds (Kim et al., 2002; Dhaked et al., 2003; Siegert and Banks, 2005; Liu et al., 2006).

The biodegradation of propionate depends on syntrophy between propionate-oxidizing bacteria and hydrogenotrophic methanogenic archaea in methanogenic environments (Worm et al., 2011). The syntrophic metabolism with other bacteria result in the pure cultivation of syntrophic propionate-oxidizing bacteria (SPOB) is very difficult. To date, only ten SPOB species have been isolated and identified (Table II). The analysis of propionate- oxidizing pathways provides information about these microorganisms in depth, including intermediates, enzymes and energy conservation. Furthermore, the genomes of several representative bacteria present the prospects to assess their unexplored functions (McInerney et al., 2007; Kosaka et al., 2008).

Propionate is always produced in anaerobic digestion and oxidized only if a syntrophic association is carried out by propionate-oxidizing bacteria and hydrogen- consumming bacteria (Chen et al., 2005; de Bok et al., 2005; Ghasimi et al., 2009). It is accumulated in anaerobic digestion process whenever, there is a change in organic loading rate, influent pH and temperature, etc., because the syntrophic propionate-oxidizing is more difficult than other intermediate products such as butyrate and ethanol (MUller et al., 2010). Thus, degradation of propionate is very important for improving performance of anaerobic digestion process. However, only a few species have been obtained by intermediate products such as butyrate and ethanol (MUller et al., 2010). Thus, degradation of propionate is very important for improving performance of anaerobic digestion process. However, only a few species have been obtained by now, leading to a lack in deep understanding of syntrophic propionate degradation.

Based on the analysis of effect of propionate accumulation on the performance of anaerobic digestion, main factors affecting its biodegradation were discussed in this work. The currently isolated SPOB and their ecophysiological, phylogenetic and genomics were focused on as well. This summary should help to isolate more SPOB and reveal the biochemical mechanism in propionate oxidation process.

Effect of propionate accunulation on anaerobic digestion: Under high operational performance, the conversion rate is proportional to the generation rate of the intermediate products, so these compounds are hardly accumulated. However, overloading, toxicity and process parameters fluctuation disturb the process and consequently cause process instable. The process imbalance generally results in accumulation of VFAs including propionate (Pullammanppallil et al., 2001). The degradation of propionate into acetate is considered as one rate limiting step in anaerobic digestion system (Amani et al., 2011a). Furthermore, its high concentration ( greater than 3000 mg L-1) may cease the fermentation process (Boone and Xun, 1987). An increase of propionate has been observed before the failure of anaerobic digesters in treating swine, municipal sludge, and food processing water (Kaspar and Wuhrmann, 1978).

Several researchers presented that propionate accumulation affect growth, diversity and activity of the methanogens. One previous research suggested that a lot of methanogens was influenced when the propionate magnitude of methanogens were decreased at the concentration of propionate above 5920 mg L-1 (Barredo and Evison, 1991). Another research also indicated that methane generation was decreased by 62~78% compared with the control at neutral pH when propionate was 5000 mg L-1 (Hajarnis and Ranade, 1994). The inhibition extent dramatically increased when the pH was decreased, indicating that undissociated propionate is the most toxic.

In addition, Dhaked et al. (2003) found a two-log reduction in methanogenic counts in the slurry fermentation at pH 6.0 or 7.0 after propionate of 15000 mg L-1 was added into slurry. They also found that methane content of biogas decreased with the increase in propionate concentration (Dhaked et al.,2003).

Factors Affecting Syntrophic Propionate Degradation pH: The pH is the most important operational parameter for anaerobic digestion processes. It has direct influence on microbial growth and metabolism. Dhaked et al. (2003) reported that the propionate anaerobic conversion is much faster at neutral or weak alkaline pH (7 to 8) than at weak acid (pH 6). Pure culture of SPOB or co-culture of SPOB and methanogens grow in a neutral environment with thepH ranged from 6 to 8.8 (Table II). We found that propionate degradation was much faster at pH 7.0 to 8.5 than that of pH 6.5 or below; the propionate anaerobic oxidation hardly occurred at pH 5.5 (unpublished data).

Temperature: Though several researchers reported that anaerobic digestion process is feasible at psychrophilic temperature, most of the reactors operate under mesophilic or thermophilic conditions (Chynoweth et al., 2000; Dhaked et al., 2003; Liu et al., 2006; Jha et al., 2011; Li et al., 2011). Thermodynamically, elevated temperature is beneficial to the conversion of acetate and then enhancing the degradation of propionate. It was reported that propionate was oxidized more swiftly at 55degC than that of at 38degC in single-stage batch anaerobic digestion of vegetable waste and wood chips (Hegde and Pullammanappallil, 2007). Thermophilic digestion was found to be a faster process as less butyrate and propionate were accumulated in comparison to a mesophilic process (Lu et al., 2007).

However, Kim et al. (2002) found that propionic acid concentration is 31 mg L-1 in the effluent at mesophilic condition when the dog food as substrate uses continuous single-stage CSTR (continuous stirred-tank reactor), but 2000 mg L-1 at thermophilic condition.

Hydrogen partial pressure: Propionate is converted into acetate and H2/CO2 that are utilized by methanogens under the methanogenic environments. Several studies showed that the high hydrogen partial pressure would seriously affect the operation of anaerobic digestion systems (Boone,1982; Harper and Pohland, 1986; Fynn and Syafila, 1990). It has been reported that the critical partial pressure for anaerobic degradation of propionate is 1x10-4 atm or 100 ppm (Wang et al., 1999; Van Lier et al., 1993; Zhang et al.,2012).

VFAs: VFAs are the important intermediates in anaerobic digestion process. Anaerobic oxidation of propionate is inhibited by VFAs and the extent of this inhibition is dependent on the VFA concentrations and pH (Siegert and Banks, 2005). These VFAs mainly contained formate, acetate, propionate and butyrate. For example, when the acetate was above 1400 mg L-1, the rate of propionate degradation was significantly decreased (Wang et al., 1999). It has been reported that an elevated acetate concentration had an inhibitory effect on the propionate-oxidizing bacteria (Boone and Xun, 1987; Hyun et al., 1998). Boone and Xun (1987) also showed that propionate degradation was severely inhibited when the 920 mg L-1 formate was added to medium with pH 7.2 (Boone and Xun, 1987). Besides acetate and formate, high propionate levels would inhibit the conversion of propionate. Amani et al. (2011b) showed the propionate had the largest inhibitory effect on the propionate removal.

The propionate removal at a propionate concentration of 2986 mg L-1 was lower than that of 1543 mg L-1 by 17% at the sludge retention time for 45 h. It was observed that higher butyric acid level also inhibits the anaerobic conversion of propionate (Amani et al., 2011b). Reactor configuration: Reactor configuration and the proximity between microbes play key roles in propionate anaerobic oxidation. Table III shows the difference of the propionate accumulation levels in treating dog food by different reactor configurations (Kim et al., 2002). In addition, propionate was competently converted into acetate in a non-mixed reactor configuration which shorted the distance of microbial consortia (Kim et al., 2002).

Apart from the above factors, some other organic compounds also inhibit the propionate conversion. For example, when oleate was added at a concentration of 0.5 g L-1 or more, both methane production and VFAs degradation stopped immediately (Angelidaki and Ahring,1992). Pullammanappallil et al. (2001) also showed that the addition of phenol caused propionate accumulation. Charateristics of SPOB: Propionate was converted by SPOB in anaerobic conditions.

SPOB are extensively present in many anaerobic ecosystems, including flooded soils, freshwater sediments, tundra, wet-wood of trees, landfills, anaerobic granular sludge and sewage digesters (Harmsen et al., 1996; Sekiguchi et al., 1999; Plugge et al.,2002; Lueders et al., 2004; McMahon et al., 2004). Fluorescence in situ hybridization reveals that a large amount of microbes, whose morphology was similar to that of Pelotomaculum thermopropionicum, a SPOB, are distributed in the internal layers of the thermophilic granule (Imachi et al., 2000). A recent study suggests that some yet uncharacterized SPOB of Smithella syntrophus clusters are present in the anaerobic digestor sludge (Ariesyady et al.,2007).

Ecophysiology: All the identified SPOB can oxidize propionate to acetate, H2/CO2 when they grow in co-culture with hydrogenotrophic methanogens under anaerobic conditions (Table II). In addition, Syntrophobacter pfennigii, Smithella propionica, Pelotomaculum thermopropionicum and Desulfotomaculum thermobenzoicum sub sp. thermosyntrophicum can also degrade some other C3 or C4 compounds, such as lactate, butanol, and butyrate (Wallrabenstein et al., 1995; Liu et al., 1999, Imachi et al.,2002; Plugge et al., 2002). Besides co-culture with methanogens, most SPOB can grow on special substrates in pure culture, such as pyruvate, fumarate, and crotonate (Nilsen et al., 1996; Liu et al., 1999; Plugge et al., 2002; Imachi et al., 2002; Chen et al., 2005).

Furthermore, the four species of Syntrophobacter and Desulfotomaculum thermocisternum have ability to axcenically grow on propionate oxidation coupling with sulfate or fumarate reduction in the deficiency of methanogens (Wallrabenstein et al., 1995; Nilsen et al., 1996; Harmsen et al., 1998; Chen et al., 2005). However, P. propionicum and P. schinkii are two obligately syntrophic bacteria which grow only in co- culture with methanogens (de Bok et al., 2005; Imachi et al.,2007). Obligately syntrophic bacteria can not link the electrons free from propionate oxidation to fumarate reduction (de Bok et al., 2005). Limited capability of SPOB to convert the substrates suggests that SPOB are specific for function and environment. The fermenting microbes with higher-level dynamics are noticeably dissimilar from those of SPOB, depending on redundance to retain the general community function (Werner et al., 2011).

This outcome suggests that biomass amendments to solve failures in propionate oxidation may be achievable in a given bioreactor, but effort to control or retain specific fermentative microbes is supposed to be very hard.

Most of the recognized SPOB degrade propionate by MMC pathway (Houwen et al., 1990; Plugge et al., 1993; Kosaka et al., 2006). Energetically, the main complicated step in propionate degradation is considered to be conversion of succinate to fumarate because of the necessity of the input energy is high. Genomic and biochemical analysis of P. thermopropionicum and Syntrophobacter fumaroxidans reveal the existence of succinate dehydrogenase gene cluster, indicating that a proton gradient across the membrane and energy input were needed to obtain proton from the exterior of the cytoplasmic membrane during the conversion of succinate to fumarate (Mclnerney et al., 2009; Stams and Plugge, 2009). S.propionica LYPT had another alternative pathway, which generates acetate and butyrate through a six-carbon intermediate (de Bok et al., 2001). But the intermediates and enzymes related to this new pathway are not been identified.

Several enzymes are involved in the MMC pathways (Kosaka et al., 2006). Amongst them, the fumarase is considered as the fundamental metabolic switch regulating the metabolism of matter and energy (Kosaka et al., 2006). The purified enzymes catalyze transformation of fumarateto malate at 70degC. In addition, inactivation of fumarase in aerobic conditions is related to the transformation of the [4Fe-4S] to the inactive [3Fe-4S] form (Shimoyama,2007).

Interspecies electron transfer is a key process for propionate degradation. In methanogenic environments, SPOB and methanogens take advantage of the metabolic abilities of their syntrophic partner to overcome energy barriers and decompose compounds that they can not be degraded by themselves. Hydrogen and formate are the primary compounds for interspecies electron transfer in methanogenic environments (Stams and Plugge, 2009). The mid-point redox potentials of the redox couples H2/H+ and formate/CO2 are similar (-414 mV and -432 mV, respectively), but hydrogen and formate have different chemical and physical properties (Thauer et al., 1977). The role of hydrogen and formate transfer in syntrophic degradation is still a matter of controversy.

For some SPOB, hydrogen transfer may be essential for interspecies electron transfer during propionate degradation (Schmidt and Ahring,1995). However, the formate transfer is more important than hydrogen in S. fumaroxidans (Dong et al., 1994). In addition, genome analysis of P. thermopropionicum reveals the presence of multiple genes encoding formate dehydrogenase (Kosaka et al., 2008). Up to now it is difficult to deduce, which one is more important in methanogenic environments. Researches with pure cultures of SPOB can shed some light on the role of hydrogen and formate in interspecies electron transfer. In particular, enzymes involved in redox reactions and the localization of electron transfer components have to be studied in more detail.

It is noteworthy that direct electron transfer might also occur by so-called nanowires (Reguera et al., 2005; Gorby et al., 2006). Nanowires may be a novel way of interspecies electron transfer taking into account the energy metabolic characteristics of SPOB, although existence of nanowires in SPOB have not been reported.

Among the ten identified SPOB, there are seven mesophilic and three thermophilic species with culturing temperature ranges of 20 to 48degC and 41 to 75degC, respectively (Table II). Some researchers (Harmsen et al.,1998; Wallrabenstein et al., 1995; Chen et al., 2005) have indicated that the favorable temperature for the mesophilic SPOB is 37degC. The favorable temperature for P.thermopropionicum and D. thermobenzoicum subsp. thermosyntrophicum is 55degC (Plugge et al., 2002; Imachi et al., 2002), while 62degC is recommended for D. thermocisternum (Nilsen et al., 1996).

Although all the identified SPOB exist in a neutral environment with the pH range from 6 to 8.8 (Table II), microorganisms accomplished syntrophic reaction were also present in extreme environments, including permanently cold soils, acidic soils, thermal springs, and alkaline soils (McInerney et al., 2009). It demonstrates that SPOB may be widely distributed at low temperature and acidophilic or basophilic environments. However, no psychrophilic or acidophilic or basophilic species have been isolated and identified. It is an opportunity and challenge to isolate SPOB from the extreme habitats in the future.

The ecophysiology of SPOB basically remained uncharted in the both natural and artificial anaerobic digestion processes as it is exceptionally difficult to isolate and culture these microbes. The oligonucleotide probes relying on the current 16S rDNA sequences of SPOB are still limited. Thus, it is very significant to isolate and identify other SPOB from all kinds of anaerobic environments.

Phylogeny of SPOB: All currently identified SPOB are grouped into two classes, which are the class d- proteobacteria in the phylum Proteobacteria and the class Clostridia within the phylum Firmicutes (Imachi et al., 2002; Plugge et al., 2002; de Bok et al., 2005) (Fig. 2). Deltaproteobacteria contained two genera Syntrophobacter and Smithella. The genus Syntrophobacter constituted a unique branch in the phylogenetic tree (Fig. 2). Low G+C Gram positive bacteria contain Desulfotomaculum and Pelotomaculum and these two genera belong to Desulfotomaculum Cluster I that is usually recognized as sulfate-reducing bacteria and have habitually been observed in different anoxic habitats (Hristova et al., 2000; Plugge et al., 2002).

Although identified SPOB are affiliated with the class d-proteobacteria or the class Clostridia, recent studies show that b-proteobacteria are the paramount community in propionate degradation process by MAR-FISH analysis in anaerobic sludge digester (Riviere et al., 2009).

Genomics of SPOB: Currently, only two SPOB have been sequenced, S. fumaroxidans and P. thermopropionicum (Kosaka et al., 2006; McInerney et al., 2007). In the catabolic pathways of P. thermopropionicum, the propionate degradation MMC pathway forms the skeleton, which connects to some external pathways. The majority of the genes coding key catabolic enzymes are essentially associated to those for PAS domain (a signaling module) regulators. It means the catabolic pathways are controlled by ecological factors and/or global cellular conditions rather than the particular substrates (Kosaka et al., 2008).

However, transcription of MMC in P. thermopropionicum was found to be substrate-dependent (Kato et al., 2009). In addition, a recent study showed that the transcription levels of two formate dehydrogenase genes in S. fumaroxidans were higher in co-culture with methanogens than in pure culture and their transcription levels were different at different substrate, indicating that the transcription of these two formate dehydrogenase genes are dependent on growth and substrate (Worm et al., 2011).


Propionate is an important intermediate product of anaerobic digestion process and its degradation is influenced by several factors including temperature, pH, reactor configuration, hydrogen partial pressure, toxins and VFAs. The accumulation of propionate has negative effects on anaerobic digestion process. As propionate degraders, SPOB occupy a unique niche in anaerobic digestion process,because of their ecological function in oxidizing propionate and then offerring substrates for methanogens. Most of the identified SPOB degrade propionate through MMC pathway and genomic information indicated the catabolic pathways are controlled by ecological factors and/or global cellular conditions.

Understanding of SPOB is limited because only ten pure cultures were obtained by now. Therefore, more SPOB should be isolated from various habitats in the future. Although it was recently suggested that direct electron transfer might also take place through so-called nanowires, the direct electron transfer between SPOB and methanogens remains to be confirmed. Ecological factors might regulate catabolic processes of SPOB, but it is not clear that how SPOB sense environmental factors to monitor cell energy levels. More research is needed on the response mechanism of SPOB to environmental factors, especially those factors regulating transcription and translation of the crucial gene in propionate degradation process. Genomics, functional genomics and culture technology are quickly rising and combining would accelerate to clarify this regulatory mechanism.

From a practical viewpoint, the quantitative and rapid detection of SPOB is essential for effective control of propionate accumulation in anaerobic digestion process.

Mathematical modeling for propionate degradation in anaerobic digester should be helpful to forecast and avoid the accumulation of propionate in time.

Acknowledgements: This work was supported by the State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology (No. 2010DX06) and National Natural Science Foundation of China (No. 51178136).


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Author:Jianzheng Li; Qiaoying Ban; Liguo Zhang; Jha, Ajay Kumar
Publication:International Journal of Agriculture and Biology
Article Type:Report
Geographic Code:9CHIN
Date:Oct 31, 2012
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