Complete genome sequence of Syntrophobacter fumaroxidans strain (MPOBT)
- Caroline M. Plugge1Email author,
- Anne M. Henstra1, 2,
- Petra Worm1,
- Daan C. Swarts1,
- Astrid H. Paulitsch-Fuchs3,
- Johannes C. M. Scholten4,
- Athanasios Lykidis5,
- Alla L. Lapidus5,
- Eugene Goltsman5,
- Edwin Kim5,
- Erin McDonald2,
- Lars Rohlin2,
- Bryan R. Crable6,
- Robert P. Gunsalus2,
- Alfons J. M. Stams1 and
- Michael J. McInerney6
© The Author(s) 2012
Published: 10 October 2012
Syntrophobacter fumaroxidans strain MPOBT is the best-studied species of the genus Syntrophobacter. The species is of interest because of its anaerobic syntrophic lifestyle, its involvement in the conversion of propionate to acetate, H2 and CO2 during the overall degradation of organic matter, and its release of products that serve as substrates for other microorganisms. The strain is able to ferment fumarate in pure culture to CO2 and succinate, and is also able to grow as a sulfate reducer with propionate as an electron donor. This is the first complete genome sequence of a member of the genus Syntrophobacter and a member genus in the family Syntrophobacteraceae. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 4,990,251 bp long genome with its 4,098 protein-coding and 81 RNA genes is a part of the Microbial Genome Program (MGP) and the Genomes to Life (GTL) Program project.
Strain MPOBT (DSM 10017) is the type strain of Syntrophobacter fumaroxidans , which is one of the four described species within the genus of Syntrophobacter . The type species of the genus Syntrophobacter is Syntrophobacter wolinii (DSM 2805) [2,3]. Strain MPOBT is currently the best-studied species in the genus Syntrophobacter. The genus name derives from the Greek words “syn”, together with “troph”, one who feeds, and “bacter”, rod shaped, referring to a rod-shaped bacterium growing in syntrophic association with hydrogen- and formate-scavenging microorganisms . The species epithet derives from the Latin word “fumaricum” pertaining to fumaric acid and the Latin adjective “oxidans”, oxidizing, referring to fumarate fermentation.
Strain MPOBT was isolated from granular sludge of a mesophilic upflow anaerobic sludge blanket (UASB) reactor, treating waste from a sugar refinery .
All currently identified syntrophic propionate-oxidizing bacteria are affiliated either with the class Deltaproteobacteria within the phylum Proteobacteria , to which Syntrophobacter belongs, or the class Clostridia within the phylum Firmicutes [5–7]. Many of the Syntrophobacter spp. are able to use sulfate as the electron acceptor for propionate oxidation and some other organic compounds and hydrogen [4,8]. In addition, they can grow by fermentation of pyruvate and fumarate. Smithella propionica is phylogenetically related to the genus Syntrophus  but lacks the ability to reduce sulfate. It also uses a different pathway to oxidize propionate distinct from that used by Syntrophobacter strains, which one that possibly involves a six-carbon intermediate. It can also grow on crotonate in pure culture [9,10].
Here we describe the features of Syntrophobacter fumaroxidans strain MPOBT together with the complete genome sequence and annotation.
Classification and features
Classification and general features of S. fumaroxidans MPOBT according to the MIGS recommendations .
Species Syntrophobacter fumaroxidans
Type strain MPOB
In pure culture: fumarate, malate, aspartate and pyruvate, fumarate + propionate, H2 + fumarate, formate + fumarate fumarate + sulfate, H2 + sulfate, formate + sulfate In syntrophy with hydrogen and formate scavenger, propionate
Propionate, fumarate, malate, aspartate, pyruvate, hydrogen, formate
Fresh water sediments, Anaerobic bioreactors
Granular sludge from a mesophilic upflow anaerobic sludge blanket UASB) reactor treating sugar refinery waste
Breda, the Netherlands
Sample collection time
Strain MPOBT utilizes propionate syntrophically via the methylmalonyl-CoA pathway in co-culture with the hydrogen and formate-utilizing methanogen, M. hungatei, and in pure culture using sulfate or fumarate as an electron acceptor [21,22]. In these cases, propionate is converted stoichiometrically to acetate and CO2 with concomitant production of methane, sulfide or succinate, respectively [1,22]. Thiosulfate also serves as an electron acceptor, but nitrate is not utilized. Strain MPOBT ferments fumarate to succinate and CO2 using the acetyl-CoA cleavage pathway , and reduces fumarate to succinate with hydrogen or formate as the electron donor [21,23].
The syntrophic species in the Syntrophobacterales can be divided in two groups based on their ability to reduce sulfate or not, which suggests an evolutionary connection between the sulfate-reducing and syntrophic lifestyles .
Two 16S rRNA gene sequences are present in the genome of strain MPOBT. Sequence analysis indicates that these two genes are almost identical (2 bp difference), and that both genes differ by up to 8 nucleotides from the previously published 16S rRNA gene sequence (X82874).
S. fumaroxidans strain MPOBT contains c- and b-type of cytochromes and the menaquinones MK-6 and MK-7 .
Genome sequencing and annotation
Genome project history
Genome sequencing project information
3kb (pUC18c), 8kb (pMCL200) and 40kb (pcc1Fos)
Gene calling method
INSDC / Genbank ID
Genbank Date of Release
October 27, 2006
NCBI project ID
Source material identifier
Genomes to Life: Bioreactors, Biotechnology, Carbon cycle, Energy production, Hydrogen production
Growth conditions and DNA isolation
S. fumaroxidans MPOBT was grown at 37oC in anaerobic bicarbonate buffered mineral salts medium as was described previously . High molecular weight genomic DNA was isolated from 2–2.5 g concentrated cell pellets using the CTAB method recommended by Joint Genome Institute (JGI), which can be found at the JGI website .
Genome sequencing and assembly
Syntrophobacter fumaroxidans genomic DNA was sequenced at JGI using a combination of 3 kb, 8 kb and 40 kb DNA libraries. All general aspects of library construction and sequencing performed at the JGI can be found at the JGI website . The Phred/Phrap/Consed software package  was used to assemble all three libraries and to assess quality [34–36]. Possible misassemblies were corrected, and gaps between contigs were closed by editing in Consed, custom primer walks or PCR amplification (Roche Applied Science, Indianapolis, IN). The error rate of the completed genome sequence of S. fumaroxidans is less than 1 in 50,000. Pair-wise graphical alignments of whole genome assemblies (e.g. synteny plots) were generated by using the MUMmer system [37,38].
Automated gene prediction was performed by using the output of Critica  complemented with the output of the Generation and Glimmer models . The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes-Expert Review platform .
% of Total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Number of replicons
Genes with function prediction
Genes in paralog clusters
Genes assigned to COGs
Genes assigned Pfam domains
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with the general COG functional categories
Translation, ribosomal structure and biogenesis
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, cell division, chromosome partitioning
Signal transduction mechanisms
Cell wall/membrane/envelope biogenesis
Intracellular trafficking, secretion, and vesicular transport
Posttranslational modification, protein turnover, chaperones
Energy production and conversion
Carbohydrate transport and metabolism
Amino acid transport and metabolism
Nucleotide transport and metabolism
Coenzyme transport and metabolism
Lipid transport and metabolism
Inorganic ion transport and metabolism
Secondary metabolites biosynthesis, transport and catabolism
General function prediction only
Not in COGs
Comparison to other genomes
Carbon flow and electron transfer
Propionyl-CoA is converted first to (S)-methylmalonyl-CoA and then to (R)-methylmalonyl-CoA by methylmalonyl-CoA epimerase (Sfum_0455), which is part of a two-gene cluster and pairs with a gene predicted to code for an ATP-dependent amino acid transport protein (Sfum_0456). This gene cluster appears immediately downstream of a two-gene cluster predicted to encode methylmalonyl-CoA mutase (Sfum_0457-8). Sfum_1223 may encode a carboxyltransferase involved in cycling carbon dioxide between the decarboxylation of oxaloacetate and the carboxylation of propionyl-CoA to form methylmalonyl-CoA. Methylmalonyl-CoA mutase (Sfum_0457-8) then converts methylmalonyl-CoA to succinyl-CoA. Removal of the CoA group is presumably accomplished by a succinyl-CoA synthetase (Sfum_1702-03), which forms succinate coupled to ATP formation from ADP and phosphate.
Succinate is then further oxidized to fumarate by a membrane-bound succinate dehydrogenase/fumarate reductase. Succinate oxidation via a menaquinone to fumarate is the most energy dependent reaction in the methyl-malonyl-CoA pathway propionate degradation to acetate in S. fumaroxidans. Succinate oxidation via menaquinone is endergonic since the midpoint potential of succinate is more positive (+30 mV) than the menaquinone (−80 mV). Therefore, the reaction requires a transmembrane proton gradient to function. Schink  calculated that about 0.66 ATP has to be invested to make this reaction energetically possible at a hydrogen partial pressure of1Pa and formate concentrations of 10 µM, which can be maintained by methanogens in a syntrophic community. The genome of S. fumaroxidans contains four gene clusters sdhABC (Sfum_1998-2000), frdABEF (Sfum_4092-4095), sdhAB-1 (Sfum_0172-0174) and sdhAB-2 (Sfum_2103-2104) with sequence similarity to succinate dehydrogenases or fumarate reductase. S. fumaroxidans might use separate enzymes for succinate oxidation and fumarate reduction. During growth with propionate plus fumarate, S. fumaroxidans needs an active fumarate reductase, whereas during growth with propionate plus sulfate, or during syntrophic growth on propionate an active succinate dehydrogenase is required .
In S. fumaroxidans, the gene cluster sdhABC (Sfum_1998-2000) codes for two cytoplasmic subunits (sdhA and B) and a five-trans-membrane (5TM) subunit containing heme (sdhC) which is similar to the type B trans-membrane subunit of Wolinella succinogenes Frd and Bacillus subtilis Sdh (Hägerhäll 1997). SdhA contains the conserved catalytic core residues and SdhB contains motifs for binding of three iron sulfur clusters, [2Fe2S], [4Fe4S], and [3Fe4S].
The gene cluster frdABEF (Sfum_4092–4095) of S. fumaroxidans lacks a gene coding for the trans-membrane subunit and is therefore classified as a type E Frd . The type E succinate:quinone oxidoreductases differ from the other four types in that they do not contain heme and have two hydrophobic subunits, SdhE and SdhF. Rather, the type E succinate:quinone oxidoreductases are more similar to those in cyanobacteria (Synechocystis) and the heterodisulfide reductases from methanogens such as Methanocaldococcus jannaschii (formerly known as Methanococcus jannaschii) . Like other gene clusters coding for E-type Frds, frdABEF contains frdE that codes for a cysteine-rich domain involved in cytochrome binding and membrane attachment . The function of the protein encoded by frdF is unknown . FrdA contains the conserved catalytic residues; FrdB contains motifs for binding of two iron sulfur clusters, [2Fe2S] and [4Fe4S]. The lack of [3Fe4S] may be compensated by iron sulfur clusters present in FrdE and F.
The third gene cluster with similarity to succinate:quinone oxidoreductases (sdhAB-1) lacks a gene coding for a transmembrane domain. SdhA contains the conserved catalytic residues and the SdhB contains a motif for [2Fe2S] iron sulfur cluster binding, but lacks motifs for [4Fe4S] or [3Fe4S] binding. Therefore, the required electron transfer via three iron-sulfur clusters cannot occur, meaning that sdhAB does not code for a conventional Sdh or Frd . Transmembrane proton transfer may occur through cytochromes for which a variety of genes are present in the genome: cytcb 561 (Sfum_0090-91); cytc 3 (Sfum_4047); cydAB-1 (Sfum_3008-09); cydAB-2 (Sfum_0338-39); cytb5 (Sfum_3227); cytb (Sfum_2932).
The fourth gene cluster is sdhAB-2 (Sfum_2103-04). These genes are part of a larger gene cluster that contains genes predicted for aconitase (Sfum_2106), citrate synthase (Sfum_2105), fumarase (Sfum_2102) and a ubiquinone prenyl transferase (Sfum_2101). These enzymes most likely function to supply biosynthetic intermediates. A 348 bp hypothetical protein (Sfum_2100) was also detected as part of this gene cluster.
The next step is the hydroxylation of fumarate forming malate (Figure. 6). Two genes for fumarase were detected in the genome. As discussed previously, a fumarase-encoding gene (Sfum_2102) is a part of a gene cluster containing aconitase, citrate synthase, succinate dehydrogenase and ubiquinone prenyl transferase encoding genes. A second fumarase-encoding gene (Sfum_2336) does not appear to be part of a gene cluster.
Malate is oxidized to oxaloacetate by malate dehydrogenase (Sfum_0460) and oxaloacetate is decarboxylated to pyruvate by pyruvate carboxyltransferase (Sfum_0461, 0676). The decarboxylation of oxaloacetate to pyruvate is concomitant with a carboxyl transfer reaction to form methylmalonyl-CoA from propionyl-CoA (Sfum_1223). Acetyl-CoA is formed from pyruvate by pyruvate ferredoxin oxidoreductase (Sfum_2792-95) and the CoA moiety is recycled to activate propionate to propionyl-CoA. Acetyl-CoA could also be converted to acetyl-phosphate and acetate by phosphotransacetylase and acetate kinase encoded by Sfum_1472-73. Formation of acetate from acetyl-phosphate could result in ATP synthesis by substrate-level phosphorylation. However, when strain MPOBT was grown on propionate, the activity of this enzyme was below detection level, suggesting that acetate was formed exclusively via an acetyl-CoA: propionate HS-CoA transferase .
Taken together, the genome reveals a complete set of genes for the conversion of propionate to acetate and carbon dioxide by the methylmalonyl-CoA pathway. Also present are genes and gene clusters for electron transfer from the key carbon oxidation steps leading to hydrogen and formate formation when S. fumaroxidans grows syntrophically (Figure. 6). These include the previously discussed fumarate reductase for quinone reduction from succinate. Menaquinol would then, ostensibly, shuttle electrons to a membrane-bound formate dehydrogenase (carbon dioxide reductase) (Sfum_0030-1) or hydrogenase complexes (Sfum_2220-22 and Sfum_2713-16). No formate dehydrogenase genes with transmembrane helices were predicted. However, several genes coding for cytochromes were detected in the genome, which do not appear to be part of larger gene clusters. These cytochromes may provide a platform for formate dehydrogenase subunits to receive electrons from the menaquinol pool. In addition, the cytochromes may also play a role in sulfate reduction, similar to Desulfovibrio sp . Reducing equivalents generated by cytosolic events, such as the oxidation of malate to oxaloacetate and pyruvate to acetyl-CoA and CO2, are probably NAD(P)H and reduced ferredoxin, respectively. Several soluble cytosolic confurcating hydrogenases (Sfum_0844-46) and formate dehydrogenases (Sfum_2703-07) probably catalyze hydrogen or formate production with the above reduced electron carriers in a mechanism proposed for hydrogen generation in Thermotoga maritima . In this mechanism the energetically favorable production of hydrogen or formate with reduced ferredoxin presumably provides the energetic input to enable the energetically unfavorable formation of hydrogen from NADH.
Strain MPOBT ferments 7 fumarate to 6 succinate and 4 CO2 in pure culture, using the acetyl-CoA cleavage pathway to oxidize fumarate to CO2 . All genes encoding for the acetyl-CoA cleavage pathway are present in the genome. In this pathway, acetyl-CoA is cleaved into a methyl-group and CO, which are both oxidized further to CO2. During propionate conversion, the pathway may be used anaplerotically to form acetyl-CoA. The genes for the acetyl-CoA pathway are scattered through the genome.
Acetyl-CoA is converted by an acetylCoA synthase/COdh complex encoded by Sfum_2564 — 2567 to CO2 and a methyl-group. The methyl group is further oxidized via 5,10-methylene tetrahydrofolate reductase (Sfum_3130), methylene-tetrahydrofolate dehydrogenase (S_fum 2686), methenyl-tetrahydrofolate cyclohydrolase (Sfum_1186), formyl-tetrafolate syntethase (Sfum_2687) and formate dehydrogenase to CO2. During complete oxidation of 1 fumarate to 4 CO2, 6 reducing equivalents are released that are used to reduce 6 fumarate to 6 succinate.
Strain MPOBT is able to couple propionate oxidation to sulfate reduction . The flow of electrons during respiratory sulfate reduction has not yet been fully described. As predicted, the genome encodes the full suite of genes necessary for dissimilatory sulfate reduction as well as several membrane complexes, which could deliver electrons from membrane electron carriers like menaquinol to cytosolic sulfate-reducing enzymes. Sulfate is first activated to adenosine-5′-phosphosulfate (APS) through the ATP dependent action of adenylylsulfate kinase. Two genes were detected that are predicted to code for adenylylsulfate kinase (Sfum_0774; 2338). Genes for APS reductase (Sfum_1047-48) were detected which likely encode the metabolic machinery necessary for the reduction of APS to sulfite and/or bisulfite. Sulfite and/or bisulfite are then reduced to sulfide by dissimilatory sulfite reductase. Alpha and beta subunits of the dissimilatory sulfite reductase were detected (Sfum_4042-43) as part of a predicted five-gene cluster along with genes that have high identity to dissimilatory sulfite reductase C (Sfum_4045). The gene organization of the alpha, beta and c-subunits of the whole cluster is different from other dissimilatory sulfate reducers . Genes predicted to encode a membrane-bound dissimilatory sulfite reductase, dsrMKJOP, were detected (Sfum_1146-50) as were the three genes encoding a quinone-interacting membrane-bound oxidoreductase (Qmo) complex (Sfum_1285-87). Additionally, qmoAB genes were detected elsewhere on the chromosome as part of a larger multi-gene cluster (Sfum_1054-59) that contains genes predicted to code for a benzoyl-CoA reductase subunit A (Sfum_1051) and three additional hypothetical proteins of unknown function (Sfum_1052-54).
Other membrane complexes include a membrane-bound, ion-translocating ferredoxin:NADH oxidoreductase (Sfum_2694-99 gene product), which could drive the unfavorable formation of reduced ferredoxin from NADH by using the ion gradient, two NADH dehydrogenases (Sfum_0199-209 and Sfum_1935-43), and two pyrophosphatases (Sfum_2995 and Sfum_3037).
Regulation and signal transduction
The S. fumaroxidans genome contains genes with similarity to those coding for a prototypical bacterial RNA core polymerase (RpoA, RpoB, RpoC) along with 12 sigma factors to confer promoter specificity. These sigma factors include one general housekeeping sigma 70 factor (RpoD), seven sigma 24 type stress related factors, two additional sigma 70-like factors, one FliA/WhiG sigma 28 type factor, and one 54 factor (RpoN) similar to that used for general nitrogen control in Escherichia coli. The genome also contains 31 genes with similarity to those coding for sigma 54-interacting transcriptional regulators (18 with response regulator signaling domains and 7 with PAS signaling domains, and 3 with GAF signaling domains), suggesting a major role for the 54-factor in global control of S. fumaroxidans gene expression. Numerous two-component regulatory systems (27 histidine kinase-type sensor transmitters, 11 response regulatory proteins, and 25 receiver-only domain proteins) are present in the genome. Compared to other Gram-negative microbes, S. fumaroxidans has a moderate number of primary transcription factors containing a helix-turn-helix motif (∼115 genes).
Motility and taxis
Unlike the thermophilic, syntrophic, propionate-utilizing, Pelotomaculum thermopropionicum SI  from the Firmicutes, S. fumaroxidans lacks genes coding for flagellar structural proteins (i.e., basal body, motor, hook, and filament) along with the associated flagellar biogenesis, anti-28 factor (FlgM) and the E. coli type master switch proteins, FlhCD or CheR, CheV, and CheC proteins. However, S. fumaroxidans contains genes for a FliA/WhiG family RNA polymerase sigma factor, nine methyl-accepting chemotaxis proteins (MCP) (three soluble and six membrane associated) with unknown roles in signal transduction plus one gene coding for each of the following signal processing proteins, CheA, CheW, CheY and CheD, and two cheB genes. Interestingly, genes for one PilQ type 4 secretion-like protein, two PilT-like retraction proteins, and PilM, PilY and PilO-like assembly proteins (one each) are predicted that may suggest alternative means of cell movement. Lastly, the absence of genes coding for pili-type nanowire proteins would suggest that direct interspecies electron transfer is unlikely .
Host defense systems
To explore possibilities of developing a genetic system for S. fumaroxidans it is crucial to investigate the mechanisms that are present in the strain that protect against foreign DNA. The genome of strain MPOBT contains two possible restriction-modification gene clusters. The first cluster consists of three genes, of which two encode the methylase and endonuclease of a Type-II restriction-modification system (Sfum_2532 and 2533, respectively) and shows high sequence identity with PstI and BsuBI restriction-modification systems. The third gene (Sfum_2534) encodes a modification requiring endonuclease which shows high sequence identity with the E. coli mrr gene, a modification-requiring restriction enzyme. The second cluster contains, two genes encoding a putative Type-III restriction modification system (Sfum_2855–2856) and three genes which do not seem to be part of the restriction-modification system. Interestingly, this system shows similarity only with hypothetical restriction-modification system coding sequences (nt-nt BLAST of both genes (endonuclease Sfum_2855 and methylase Sfum_2856): Candidatus Desulforudis audaxviator MP104C, 72% coverage; Chlorobium limicola DSM 245, 72% coverage; Cellvibrio japonicus Ueda107, 43% coverage; Verminephrobacter eiseniae EF01-2, 67% coverage). Since the genes do not show high sequence identity with described systems, it is not possible to predict the specificity of the system.
Additionally, the genome of strain MPOBT harbors genes encoding two CRISPR/Cas systems. The first system (Sfum_1345-1356) can be classified as a type I-E system associated with a 69-spacer CRISPR locus, the second (Sfum_2824-2831) as type III-A system and is associated with a CRISPR locus containing 79 spacers .
Taken together, strain MPOBT has multiple systems to protect itself against foreign DNA, making it a challenge to develop a genetic system for this strain.
The European authors were financially supported by the Earth and Life Sciences division (ALW 814.02.017) and Chemical Science division (CW 700.55.343) of the Netherlands Organization for Scientific Research (NWO). CMP was supported by a short-term personal fellowship of the Netherlands Genome Initiative (NGI 050-72-408). Annotation assistance provided by Dr. McInerney’s group was supported by grant DE-FG02-96ER20214 from the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the US Department of Energy and genomic analyses provided by Dr. Gunsalus’ group were supported by US Department of Energy grant DE-FG03-86ER13498 and the UCLA-DOE Institute of Genomics and Proteomics.
- Harmsen HJM, VanKuijk BLM, Plugge CM, Akkermans ADL, DeVos WM, Stams AJM. Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 1998; 48:1383–1387. PubMed http://dx.doi.org/10.1099/00207713-48-4-1383View ArticlePubMedGoogle Scholar
- McInerney MJ, Stams AJM, Boone DR. Genus Syntrophobacter. In: Staley JT, Boone DR, Brenner DJ, de Vos P, Garrity GM, Goodfellow M, Krieg NR, Rainey, FA, Schleifer KH (eds) Bergey’s Manual of Systematic Bacteriology, second edition, vol 2 2005; Springer, NY, pp 1021–1027.View ArticleGoogle Scholar
- Boone DR, Bryant MP. Propionate-degrading bacterium, Syntrophobacter wolinii sp. nov., gen. nov., from methanogenic ecosystems. Appl Environ Microbiol 1980; 40:626–632. PubMedPubMed CentralPubMedGoogle Scholar
- McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B, Rohlin L, Gunsalus R. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 2008; 1125:58–72. PubMed http://dx.doi.org/10.1196/annals.1419.005View ArticlePubMedGoogle Scholar
- Imachi H, Sekiguchi Y, Kamagata Y, Hanada S, Ohashi A Harada H. Pelotomaculum thermopropionicum gen. nov., sp. nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 2002; 52:1729–1735. PubMed http://dx.doi.org/10.1099/ijs.0.02212-0PubMedGoogle Scholar
- Plugge CM, Balk M, Stams AJM. Desulfotomaculum thermobenzoicum subsp. thermosyntrophicum subsp. nov., a thermophilic syntrophic propionate-oxidizing spore-forming bacterium. Int J Syst Evol Microbiol 2002; 52:391–399. PubMedView ArticlePubMedGoogle Scholar
- de Bok FAM, Harmsen HJM, Plugge CM, deVries MC, Akkermans ADL, de Vos WM, Stams AJM. The first true obligately syntrophic propionate-oxidizing bacterium, Pelotomaculum schinkii sp. nov., co-cultured withMethanospirillum hungatei, and emended description of the genus Pelotomaculum. Int J Syst Evol Microbiol 2005; 55:1697–1703. PubMed http://dx.doi.org/10.1099/ijs.0.02880-0View ArticlePubMedGoogle Scholar
- Plugge CM, Zhang W, Scholten JCM, Stams AJM. Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2011; 2:81. PubMedPubMed CentralView ArticlePubMedGoogle Scholar
- Liu Y, Balkwill DL, Aldrich HC, Drake GR, Boone DR. Characterization of the anaerobic propionate-degrading syntrophs Smithella propionica gen. nov., sp. nov. and Syntrophobacter wolinii. Int J Syst Bacteriol 1999; 49:545–556. PubMed http://dx.doi.org/10.1099/00207713-49-2-545View ArticlePubMedGoogle Scholar
- De Bok FAM, Stams AJM, Dijkema C, Boone DR. Pathway of propionate oxidation by a syntrophic culture of Smithella propionica and Methanospirillum hungatei. Appl Environ Microbiol 2001; 67:1800–1804. PubMed http://dx.doi.org/10.1128/AEM.67.4.1800-1804.2001PubMed CentralView ArticlePubMedGoogle Scholar
- Field D, Garrity G, Gray T, Morrison N, Selengut J, Sterk P, Tatusova T, Thomson N, Allen MJ, Angiuoli SV, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 2008; 26:541–547. PubMed http://dx.doi.org/10.1038/nbt1360PubMed CentralView ArticlePubMedGoogle Scholar
- Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domainsArchaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 1990; 87:4576–4579. PubMed http://dx.doi.org/10.1073/pnas.87.12.4576PubMed CentralView ArticlePubMedGoogle Scholar
- Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part B, Springer, New York, 2005, p. 1.View ArticleGoogle Scholar
- Validation List no. 107. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2006; 56:1–6. PubMed http://dx.doi.org/10.1099/ijs.0.64188-0
- Kuever J, Rainey FA, Widdel F. Class IV. Deltaproteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part C, Springer, New York, 2005, p. 922.View ArticleGoogle Scholar
- Kuever J, Rainey FA, Widdel F. Order VI. Syntrophobacterales ord. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part C, Springer, New York, 2005, p. 1021.Google Scholar
- Kuever J, Rainey FA, Widdel F. Family I. Syntrophobacteraceae fam. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT (eds), Bergey’s Manual of Systematic Bacteriology, Second Edition, Volume 2, Part C, Springer, New York, 2005, p. 1021.Google Scholar
- Validation List no. 15. Validation of the publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol 1984; 34:355–357. http://dx.doi.org/10.1099/00207713-34-3-355
- Chen S, Liu X, Dong X. Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors. Int J Syst Evol Microbiol 2005; 55:1319–1324. PubMed http://dx.doi.org/10.1099/ijs.0.63565-0View ArticlePubMedGoogle Scholar
- Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene Ontology: tool for the unification of biology. Nat Genet 2000; 25:25–29. PubMed http://dx.doi.org/10.1038/75556PubMed CentralView ArticlePubMedGoogle Scholar
- Plugge CM, Dijkema C, Stams AJM. Acetyl-CoA cleavage pathway in a syntrophic propionate oxidizing bacterium growing on fumarate in the absence of methanogens. FEMS Microbiol Lett 1993; 110:71–76. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06297.xView ArticleGoogle Scholar
- Van Kuijk BLM, Stams AJM. Sulfate reduction by a syntrophic propionate-oxidizing bacterium. Antonie van Leeuwenhoek 1995; 68:293–296. PubMed http://dx.doi.org/10.1007/BF00874139View ArticlePubMedGoogle Scholar
- Stams AJM, vanDijk JB, Dijkema C, Plugge CM. Growth of syntrophic propionate-oxidizing bacteria with fumarate in the absence of methanogenic bacteria. Appl Environ Microbiol 1993; 59:1114–1119. PubMedPubMed CentralPubMedGoogle Scholar
- Pagani I, Liolios K, Jansson J, Chen IM, Smirnova T, Nosrat B, Markowitz VM, Kyrpides NC. The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 2012; 40:D571–D579. PubMed http://dx.doi.org/10.1093/nar/gkr1100PubMed CentralView ArticlePubMedGoogle Scholar
- Stams AJM, Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 2009; 7:568–577. PubMed http://dx.doi.org/10.1038/nrmicro2166View ArticlePubMedGoogle Scholar
- Loy A, Küsel K, Lehner A, Drake HL, Wagner M. Microarray and functional gene analyses of sulfate-reducing prokaryotes in low sulfate, acidic fens reveal co-occurence of recognized genera and novel lineages. Appl Environ Microbiol 2004; 70:6998–7009. PubMed http://dx.doi.org/10.1128/AEM.70.12.6998-7009.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Lueders T, Pommerenke B, Friedrich MW. Stable-Isotope Probing of microorganisms thriving at thermodynamic limits: syntrophic propionate oxidation in flooded soil. Appl Environ Microbiol 2004; 70:5778–5786. PubMed http://dx.doi.org/10.1128/AEM.70.10.5778-5786.2004PubMed CentralView ArticlePubMedGoogle Scholar
- Imachi H, Sekiguchi Y, Kamagata Y, Loy A, Qiu YL, Hugenholtz P, Kimura N, Wagner M, Ohashi A, Harada H. Non-sulfate-reducing, syntrophic bacteria affiliated with Desulfotomaculum Cluster I are widely distributed in methanogenic environments. Appl Environ Microbiol 2006; 72:2080–2091. PubMed http://dx.doi.org/10.1128/AEM.72.3.2080-2091.2006PubMed CentralView ArticlePubMedGoogle Scholar
- Wallrabenstein C, Hauschild E, Schink B. Syntrophobacter pfennigii sp. nov., new syntrophically propionate-oxidizing anaerobe growing in pure culture with propionate and sulfate. Arch Microbiol 1995; 164:346–352. http://dx.doi.org/10.1007/BF02529981View ArticleGoogle Scholar
- Chen SY, Liu XL, Dong XZ. Syntrophobacter sulfatireducens sp. nov., a novel syntrophic, propionate-oxidizing bacterium isolated from UASB reactors. Int J Syst Evol Microbiol 2005; 55:1319–1324. PubMed http://dx.doi.org/10.1099/ijs.0.63565-0View ArticlePubMedGoogle Scholar
- Syntrophobacter fumaroxidans taxon id. http://img.jgi.doe.gov/cgi-bin/w/main.cgi?page=taxon Detail&taxon oid=63 9633063
- DOE Joint Genome Institute. http://www.jgi.doe.gov
- Phred/Phrap/Consed software package. http://www.phrap.org
- Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 1998; 8:186–194. PubMedView ArticlePubMedGoogle Scholar
- Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998; 8:175–185. PubMedView ArticlePubMedGoogle Scholar
- Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998; 8:195–202. PubMedView ArticlePubMedGoogle Scholar
- Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999a; 27:4636–4641. PubMed http://dx.doi.org/10.1093/nar/27.23.4636PubMed CentralView ArticlePubMedGoogle Scholar
- Delcher AL, Kasif S, Fleischmann RD, Peterson J, White O, Salzberg SL. Alignment of whole genomes. Nucleic Acids Res 1999b; 27:2369–2376. PubMed http://dx.doi.org/10.1093/nar/27.11.2369PubMed CentralView ArticlePubMedGoogle Scholar
- Badger JH, Olsen GJ. CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol 1999; 16:512–524. PubMed http://dx.doi.org/10.1093/oxfordjournals.molbev.a 026133View ArticlePubMedGoogle Scholar
- Markowitz VM, Mavromatis K, Ivanova NN, Chen IMA, Chu K, Kyrpides NC. IMG ER: a system for microbial genome annotation expert review and curation. Bioinformatics 2009; 25:2271–2278. PubMed http://dx.doi.org/10.1093/bioinformatics/btp393View ArticlePubMedGoogle Scholar
- von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, Foglierini M, Jouffre N, Huynen MA, Bork P. STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res 2005; 33:D433–D437. PubMed http://dx.doi.org/10.1093/nar/gki005View ArticleGoogle Scholar
- STRING. http://string.embl.de/.
- Scholten JCM, Culley DE, Brockman FJ, Wu G, Zhang W. Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: Involvement of an ancient horizontal gene transfer. Biochem Biophys Res Commun 2007; 352:48–54. PubMed http://dx.doi.org/10.1016/j.bbrc.2006.10.164View ArticlePubMedGoogle Scholar
- Schink B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 1997; 61:262–280. PubMedPubMed CentralPubMedGoogle Scholar
- Lancaster CRD. Succinate:quinone oxidoreductases: an overview. Biochim Biophys Acta 2002; 1553:1–6. PubMed http://dx.doi.org/10.1016/S0005-2728(01)00240-7View ArticlePubMedGoogle Scholar
- Lemos RS, Fernandes AS, Pereira MM, Gomes CM, Teixeira M. Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centers and membrane attachment. Biochim Biophys Acta 2002; 1553:158–170. PubMed http://dx.doi.org/10.1016/S0005-2728(01)00239-0View ArticlePubMedGoogle Scholar
- Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, et al. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 2004; 22:554–559. PubMed http://dx.doi.org/10.1038/nbt959View ArticlePubMedGoogle Scholar
- Schut GJ, Adams MW. The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 2009; 191:4451–4457. PubMed http://dx.doi.org/10.1128/JB.01582-08PubMed CentralView ArticlePubMedGoogle Scholar
- Pereira IA, Ramos AR, Grein F, Marques MC, Marques da Silva M, Venceslau SS. A comparative genome analysis of energy metabolism in sulfate reducing bacteria and archaea. Front Microbiol 2011; 2:69. PubMedPubMed CentralPubMedGoogle Scholar
- Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA 2006; 103:11358–11363. PubMed http://dx.doi.org/10.1073/pnas.0604517103PubMed CentralView ArticlePubMedGoogle Scholar
- Makarova KS, Haft DH, Barrangou R, Brouns SJJ, Charpentier E, Horvath P, Moineau S, Mojica FJM, Wolf YI, Yakunin AF, et al. Evolution and classification of the CRISPR-Cas systems. Nat Microbiol Rev 2011; 9:467–477. PubMed http://dx.doi.org/10.1038/nrmicro2577View ArticleGoogle Scholar