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Metabolic Flexibility of Sulfate-Reducing Bacteria View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Wageningen University & Research Publications REVIEW ARTICLE published: 02 May 2011 doi: 10.3389/fmicb.2011.00081 Metabolic flexibility of sulfate-reducing bacteria Caroline M. Plugge1*, Weiwen Zhang 2, Johannes C. M. Scholten3 and Alfons J. M. Stams1 1 Laboratory of Microbiology, Wageningen University, Wageningen, Netherlands 2 Center for Ecogenomics, Biodesign Institute, Arizona State University, Tempe, AZ, USA 3 230 King Fisher Court, Harleysville, PA, USA Edited by: Dissimilatory sulfate-reducing prokaryotes (SRB) are a very diverse group of anaerobic bacteria Thomas E. Hanson, University of that are omnipresent in nature and play an imperative role in the global cycling of carbon and Delaware, USA sulfur. In anoxic marine sediments sulfate reduction accounts for up to 50% of the entire organic Reviewed by: Lee Krumholz, University of Oklahoma, mineralization in coastal and shelf ecosystems where sulfate diffuses several meters deep USA into the sediment. As a consequence, SRB would be expected in the sulfate-containing upper Ralf Rabus, University Oldenburg, sediment layers, whereas methanogenic archaea would be expected to succeed in the deeper Germany sulfate-depleted layers of the sediment. Where sediments are high in organic matter, sulfate *Correspondence: is depleted at shallow sediment depths, and biogenic methane production will occur. In the Caroline M. Plugge, Laboratory of Microbiology, Wageningen University, absence of sulfate, many SRB ferment organic acids and alcohols, producing hydrogen, acetate, Dreijenplein 10, 6703 HB Wageningen, and carbon dioxide, and may even rely on hydrogen- and acetate-scavenging methanogens to Netherlands. convert organic compounds to methane. SRB can establish two different life styles, and these e-mail:[email protected] can be termed as sulfidogenic and acetogenic, hydrogenogenic metabolism. The advantage of having different metabolic capabilities is that it raises the chance of survival in environments when electron acceptors become depleted. In marine sediments, SRB and methanogens do not compete but rather complement each other in the degradation of organic matter. Also in freshwater ecosystems with sulfate concentrations of only 10–200 μM, sulfate is consumed efficiently within the top several cm of the sediments. Here, many of the δ-Proteobacteria present have the genetic machinery to perform dissimilatory sulfate reduction, yet they have an acetogenic, hydrogenogenic way of life. In this review we evaluate the physiology and metabolic mode of SRB in relation with their environment. Keywords: sulfate-reducing bacteria, metabolic flexibility, syntrophy, metabolic interactions Dissimilatory sulfate-reducing prokaryotes (SRB) are a diverse sulfate-depleted environments, it is possible that sulfate reducers group of anaerobic bacteria that are widespread in nature and play may be metabolically active by living in association with metha- an essential role in the global cycling of carbon and sulfur. The SRB nogenic bacteria instead of reducing sulfate (Bryant et al., 1977; mainly use sulfate, the most oxidized form of sulfur, as the terminal McInerney et al., 1981). This symbiotic process is known as “syn- electron acceptor in the oxidation of hydrogen and various organic trophy” and is a widespread type of microbial interaction especially compounds (Widdel and Hansen, 1991; Rabus et al., 2006; Muyzer in methanogenic environments (Bryant et al., 1967; Schink, 1997; and Stams, 2008). Some SRB can use nitrate as electron acceptor, Stams and Plugge, 2009). Two major life styles are thus performed and their possible microaerophilic nature has also been discussed by some SRB: the sulfidogenic and the syntrophic metabolism. (Cypionka, 2000). The advantage of having different metabolic potentials is that it The anaerobic food chain changes largely when sulfate enters enhances the chance of survival of communities of SRB in environ- the methanogenic zone. In that case sulfate-reducing bacteria will ments when electron acceptors become depleted. outcompete methanogenic archaea for hydrogen, formate and ace- In sulfate-depleted marine sediments, SRB and methanogens do tate, and syntrophic methanogenic communities for substrates like not compete but rather complement each other in the degradation propionate and butyrate (Stams, 1994; Muyzer and Stams, 2008). of organic matter. Also in sulfate-rich marine sediments, SRB and Interestingly, sulfate reducers can also grow without sulfate and in methanogens co-exist, but presumably by competing for common some cases they grow only in syntrophic association with metha- substrates, such as H2 (Oremland et al., 1982; Winfrey and Ward, nogens or other hydrogen-scavengers. Thus, sulfate reducers may 1983; Kuivila et al., 1990; Holmer and Kristensen, 1994). Recently, compete with methanogens and grow in syntrophy with metha- it was found that sulfate reducers were still abundant in the metha- nogens depending on the prevailing environmental conditions nogenic zones of Aarhus Bay (Leloup et al., 2009). (Muyzer and Stams, 2008). Already in the 1970s, the metabolic flex- In the past decades significant progress has been made through ibility of SRB was investigated. Bryant et al. (1977) demonstrated extensive studies of pure cultures, in SRB particularly with its model growth of Desulfovibrio on lactate in the absence of sulfate but in species Desulfovibrio vulgaris. Genomic analysis gave insight how the presence of a methanogen. They concluded that the sulfate the utilization of H2 and organic acids (formate and lactate) as reducer produced H2 which is used by the methanogen, acting as electron donors is coupled to sulfate reduction, ATP synthesis and an alternative electron sink in the absence of sulfate. Therefore, in growth (Heidelberg et al., 2004). Lactate is oxidized through several www.frontiersin.org May 2011 | Volume 2 | Article 81 | 1 Plugge et al. Metabolic flexibility of sulfate-reducing bacteria enzymatic steps to acetate resulting in ATP synthesis (Heidelberg excreted by the other species. The results of these initial model et al., 2004). Besides substrate-level ATP synthesis, additional ATP simulations predicted that D. vulgaris, growing optimally, converts is generated from a proton gradient according to a chemiosmotic the majority of the carbon contained in the substrate lactate into model (Peck, 1966), in which the protons and electrons produced acetate, and that only 4.8% of the carbon is directed to biomass. during lactate oxidation react with cytoplasmic hydrogenases to The remaining carbon is lost as CO2 or formate. To maintain redox form H2, which then diffuses across the membrane where it is re- balance in the absence of an external electron acceptor, evolution oxidized by periplasmic hydrogenases to form a proton gradient of a reduced compound, either formate or hydrogen, is predicted. (Odom and Peck, 1981; Heidelberg et al., 2004). The electrons gen- The model shows that when acetate is available, it is the preferred erated during lactate oxidation are channeled to sulfate through source of biomass carbon for M. maripaludis over the CO dehydro- a vast network of hemes that is created by various interconnected genase pathway to fix carbon dioxide. This prediction is consistent c-type cytochromes and involving several transmembrane com- with published data and the experimental results showed that M. plexes (Aubert et al., 2000; Heidelberg et al., 2004). Nowadays, maripaludis consumes acetate and presumably uses it as a carbon research efforts with SRB are significantly aided by the availability source (Stolyar et al., 2007). of over 20 genome sequences of which 12 representatives of the Comparative transcriptomic analysis to investigate syntrophic genus Desulfovibrio (http://img.jgi.doe.gov; Integrated Microbial systems was done recently. In one study, comparative transcrip- Genomes). Numerous research groups have since then reported tional analysis of D. vulgaris in two culture conditions was per- global transcriptomic and proteomic analyses of D. vulgaris under formed: syntrophic co-cultures with M. maripaludis strain S2 various growth or stress conditions (Chhabra et al., 2006; Clark (without sulfate) and sulfate-limited monocultures (Walker et al., 2006; He et al., 2006; Mukhopadhyay et al., 2006, 2007; Zhang et al., 2009). During syntrophic growth on lactate with a hydrog- et al., 2006a,b,c; Bender et al., 2007; Tang et al., 2007; Pereira et al., enotrophic methanogen, numerous genes involved in electron 2008; Walker et al., 2009; Plugge et al., 2010). As a result, there has transfer and energy generation were up-regulated in D. vulgaris been a better understanding of the electron transfer and energy con- compared with their expression in sulfate-limited pure cultures. servation mechanisms of D. vulgaris mainly associated with lactate In another study, whole-genome D. vulgaris microarrays were used oxidation during sulfidogenic growth. Yet, the energy metabolism to determine relative transcript levels when D. vulgaris shifted of D. vulgaris is very complex and flexible and as such deserves its lifestyle from syntroph in a lactate-oxidizing co-culture with further study (Pereira et al., 2008). Methanosarcina barkeri to a sulfidogenic lifestyle (Plugge et al., While the physiology of the symbiotic/syntrophic relationship 2010). In the study, syntrophic co-cultures were grown in two has been studied for more than 40 years (Bryant
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