Genome analysis of Desulfotomaculum gibsoniae strain GrollT a highly versatile Gram-positive sulfate-reducing bacterium
- Jan Kuever1,
- Michael Visser2,
- Claudia Loeffler3,
- Matthias Boll3,
- Petra Worm2,
- Diana Z. Sousa2,
- Caroline M. Plugge2,
- Peter J. Schaap4,
- Gerard Muyzer5,
- Ines A. C. Pereira6,
- Sofiya N. Parshina7,
- Lynne A. Goodwin8, 9,
- Nikos C. Kyrpides8,
- Janine Detter9,
- Tanja Woyke8,
- Patrick Chain8, 9,
- Karen W. Davenport8, 9,
- Manfred Rohde10,
- Stefan Spring11,
- Hans-Peter Klenk11 and
- Alfons J. M. Stams2, 12
© The Author(s) 2014
Published: 15 June 2014
Desulfotomaculum gibsoniae is a mesophilic member of the polyphyletic spore-forming genus Desulfotomaculum within the family Peptococcaceae. This bacterium was isolated from a freshwater ditch and is of interest because it can grow with a large variety of organic substrates, in particular several aromatic compounds, short-chain and medium-chain fatty acids, which are degraded completely to carbon dioxide coupled to the reduction of sulfate. It can grow autotrophically with H2 + CO2 and sulfate and slowly acetogenically with H2 + CO2, formate or methoxylated aromatic compounds in the absence of sulfate. It does not require any vitamins for growth. Here, we describe the features of D. gibsoniae strain GrollT together with the genome sequence and annotation. The chromosome has 4,855,529 bp organized in one circular contig and is the largest genome of all sequenced Desulfotomaculum spp. to date. A total of 4,666 candidate protein-encoding genes and 96 RNA genes were identified. Genes of the acetyl-CoA pathway, possibly involved in heterotrophic growth and in CO2 fixation during autotrophic growth, are present. The genome contains a large set of genes for the anaerobic transformation and degradation of aromatic compounds, which are lacking in the other sequenced Desulfotomaculum genomes.
Keywordsspore-forming anaerobes sulfate reduction autotrophic anaerobic degradation of aromatic compounds complete oxidizer Peptococcaceae Clostridiales
Desulfotomaculum gibsoniae strain GrollT (DSM 7213) is a mesophilic sulfate-reducing bacterium isolated from a freshwater ditch in Bremen, Northern Germany [1,2]. It grows with a wide range of substrates, including organic acids, such as medium-chain fatty acids, short-chain fatty acids, and several aromatic compounds . These substrates are degraded to CO2 coupled to sulfate reduction. The strain is also able to grow autotrophically with H2/CO2 and sulfate, and is able to ferment pyruvate and crotonate. In the absence of sulfate, it grows slowly on H2/CO2, formate, and methoxylated aromatic compounds. D. gibsoniae does not require vitamins for growth.
The genus Desulfotomaculum is a heterogeneous group of anaerobic spore-forming sulfate-reducing bacteria, with thermophilic, mesophilic, and psychrophilic members that grow at neutral or alkaline pH values . Their cell wall stains Gram-negative, but the ultrastructure of the cell wall is characteristic of Gram-positive bacteria . They are physiologically very diverse. In contrast to Gram-negative sulfate-reducing bacteria and closely related Clostridia, very little is known about their physiology, but members of this genus are known to play an important role in the carbon and sulfur cycle in diverse habitats.
The Desulfotomaculum genus is divided phylogenetically into different subgroups . To get a thorough understanding of the evolutionary relationships of the different Desulfotomaculum subgroups and the physiology of the individual species, it is important to have genome sequence information. Here, we present a summary of the features of D. gibsoniae strain GrollT, together with the description of the complete genomic sequencing and annotation. A special emphasis is put on the ability of this strain to grow on a large variety of aromatic compounds and the responsible genes, and its capacity for acetogenic growth in the absence of sulfate.
Classification and features
Classification and general features of D. gibsoniae strain GrollT (DSM 7213) according to the MIGS recommendations .
Species Desulfotomaculum gibsoniae
Type strain Groll
Negative with a Gram-positive cell wall structure
Straight or slightly curved rods with pointed ends
Motile, but motility was lost during cultivation
Spherical and central, slightly swelling the cell
CO2 (autotrophic) and many organic compounds including aromatic compounds
Sulfate-dependent growth and fermentative growth with pyruvate, crotonate, formate, H2 + CO2, and methoxylated aromatic compounds
Electron acceptor Habitat
Sulfate, thiosulfate and sulfite
Fresh water, mud, soil
0–35 g l−1, no addition of NaCl necessary
BSF 1 
Grolland, Bremen, Germany
Sample collection time
60 cm (water), 1 cm sediment
Genome sequencing and annotation
Genome project history
Genome sequencing project information
Three genomic libraries: one Illumina shotgun library, one 454 standard library, and one paired end 454 library
Illumina GAii, 454 Titanium
479 × Illumina; 27.2 × pyrosequence
Newbler v. 2.3
Gene calling method
Genbank Date of Release
May 13, 2013
NCBI project ID
Source material identifier
Obtain insight into the phylogenetic and physiological diversity of Desulfotomacum species, and genes for anaerobic degradation of aromatic compounds
Growth conditions and DNA isolation
D. gibsoniae strain GrollT, DSM 7213, was grown anaerobically in DSMZ medium 124a (Desulfotomaculum Groll Medium) [2,20] at 35°C. DNA was isolated from 0.5–1 g of cell paste using Jetflex Genomic DNA Purification kit (GENOMED 600100) following the standard protocol as recommended by the manufacturer. DNA quality was inspected according the guidelines of the genome sequence laboratory.
Genome sequencing and assembly
The genome was sequenced using a combination of Illumina and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website . Pyrosequencing reads were assembled using the Newbler assembler (Roche). The initial Newbler assembly consisting of 139 contigs in one scaffold was converted into a phrap  assembly by making fake reads from the consensus, to collect the read pairs in the 454 paired end library. Illumina GAii sequencing data (2,432 Mb) was assembled with Velvet  and the consensus sequences were shredded into 1.5 kb overlapped fake reads and assembled together with the 454 data. The 454 draft assembly was based on 220 Mb 454 draft data and all of the 454 paired end data. Newbler parameters are -consed -a 50 -l 350 -g -m -ml 21. The Phred/Phrap/Consed software package  was used for sequence assembly and quality assessment in the subsequent finishing process. After the shotgun stage, reads were assembled with parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with gapResolution , Dupfinisher , or sequencing cloned bridging PCR fragments with subcloning. Gaps between contigs were closed by editing in Consed, by PCR and by Bubble PCR primer walks (J.-F. Chang, unpublished). A total of 132 additional reactions were necessary to close some gaps and to raise the quality of the final contigs. Illumina reads were also used to correct potential base errors and increase consensus quality using a software Polisher developed at JGI . The error rate of the final genome sequence is less than 1 in 100,000. Together, the combination of the Illumina and 454 sequencing platforms provided 506.2 × coverage of the genome. The final assembly is based on 2,347 Mb of Illumina draft data and 133 Mb of pyrosequence draft data.
Genes were identified using Prodigal  as part of the DOE-JGI genome annotation pipeline , followed by a round of manual curation using the JGI GenePRIMP pipeline . The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) non-redundant database, UniProt, TIGR-Fam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform .
% of total
Genome size (bp)
DNA coding region (bp)
DNA G+C content (bp)
Genes in paralog clusters
Genes assigned to COGs
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with the general COG functional categories
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, mitosis and meiosis
Signal transduction mechanisms
Cell wall/membrane biogenesis
Intracellular trafficking and secretion
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
Insights into the genome
Degradation of aromatic compounds
In sulfate-reducing bacteria (e.g. Desulfobacula toluolica) methylated aromatic compounds such as toluenes, xylenes or cresols are thought to be degraded via an initial fumarate addition to the methyl group followed by β-oxidation-like reactions [32–34]. The genes putatively coding for the enzyme catalyzing the fumarate addition reaction (hbsABC) are present in two copies in the genome of D. gibsoniae. They might have different substrate specificities for the growth substrates m- and p-cresol since the genome of D. toluolica possesses one set of these genes and can only grow with p-cresol [34,35]. In D. gibsoniaem- and p-cresol are expected to be converted to 3- or 4-hydroxybenzylsuccinate. The genes coding for enzymes involved in the subsequent β-oxidation (bhsABCDEFGH), yielding 3- or 4-hydroxybenzoyl-CoA, are also present in two copies. In growth experiments toluene degradation was not observed for D. gibsoniae [1,2]. The genome provides no opposing information. All genes for the degradation of the growth substrates phenylacetate and phenol are present including the type of phenylphosphate carboxylase typically found in strict anaerobes .
All genes encoding enzymes of the upper benzoyl-CoA degradation pathway were identified in D. gibsoniae. The growth substrate benzoate is activated to benzoyl-CoA either via ATP-dependent CoA-ligase (bcl) or succinyl-CoA dependent CoA-transferase (bct) [37,38]. There are two classes of dearomatizing benzoyl-CoA reductases (BCRs) . Class I are ATP-dependent FeS enzymes composed of four different subunits . There are two subclasses of ATP-dependent BCRs of the Thauera- and the Azoarcus-type. ATP-independent class II BCRs contain eight subunits and harbor a tungsten-containing cofactor in the active site . The ATP-independent class II BCR is characteristic of strictly anaerobic aromatic compound degrading bacteria . In D. gibsoniae the genes of the catalytic subunit (bamB) of the class II BCR are present in six copies. All of the predicted seven genes for the putative electron activating subunits of class II BCR (bamCDEFGHI) were identified in at least two copies and arranged next to each other. Surprisingly, genes of a class I BCR with high similarity (47–68% amino acid identity) to class I BCRs of the Azoarcus-type (bzdNOPQ) were found, but these were not located in a single transcriptional unit. It is unclear which of the putative BCR-encoding genes is used for benzoyl-CoA and/or 3-OH-benzoyl-CoA reduction. The genes necessary to convert the product of BCRs, a cyclic conjugated dienoyl-CoA, to 3-OH-pimelyl-CoA via modified β-oxidation (dch, had, oah) are present in one copy each. It is unclear whether these genes are also involved in 3-OH-benzoyl-CoA degradation. One of the more unusual growth substrates of D. gibsoniae is catechol, a substrate metabolized only by a very limited number of anaerobic bacteria. The pathway of catechol metabolism via protocatechuate was outlined 20 years ago  and is now confirmed by the genome analysis. For the degradation of lignin monomers, the side chains will be degraded and the methoxy-group will be removed by o-demethylation. The genes responsible for this mechanism are present in the genome (Desgi_0674 to Desgi_0676). The resulting compounds can then be degraded by the pathways outlined in Figure 4.
Complete substrate oxidation, autotrophic growth and homoacetogenic growth
C1 compound degradation
In addition to the three cooS genes downstream of the genes coding for the acetyl-CoA synthase, D. gibsoniae has two other cooS genes in its genome, Desgi_2753, and Desgi_3080. The latter has a transcriptional regulator (Desgi_3081) downstream and a ferredoxin (Desgi_3079) and a nitrite reductase (Desgi_3078) upstream. Growth tests on CO have not yet been performed. However, the presence of multiple cooS genes with neighbor genes like ferredoxin and nitrate reductase, or genes coding for the acetyl-CoA pathway indicates that D. gibsoniae may grow on CO.
D. gibsoniae can grow on formate coupled to sulfate reduction. In the genome, two putative formate dehydrogenases (FDHs) were found. One FDH (Desgi_1522-23) is translocated over the membrane and bound to a polysulfide reductase (NrfD)-like protein containing 10 trans-membrane helixes (Desgi_1524). The alpha subunit contains a twin-arginine translocation (tat) motif and genes encoding proteins of the Tat system; TatA (Desgi_1521) and TatC (Desgi_1526) were found near the alpha subunit coding gene. The second FDH (Desgi_2136-2139) might be a confurcating FDH. Desgi_2138 shows similarity with the NADH binding 51kD subunit of NADH:ubiquinone oxidoreductase and Fe-S cluster binding motifs, which were found in all subunits.
No methanol methyltransferase genes can be found in the genome of D. gibsoniae, which correlates with the absence of growth on methanol . Other methyltransferase genes that might point to growth with methylated amines were not found, except for a possible dimethylamine methyltransferase beta subunit (Desgi_3904) and a cobalamin binding protein (Desgi_3903). However, another methyltransferase gene, mtbA, which is absent from the genome, is necessary for growth with dimethylamine.
Propionate and butyrate oxidation
The genome contains single copies of the sulfate adenyltransferase (Desgi_3703), adenosine-5´-phosphosulfate (APS) reductase (Desgi_3701–3702) and dissimilatory sulfite reductase (Desgi 4661–4662) as are found in most of the other members of the genus [18–20]. A membrane-bound pyrophosphatase (Desgi_4294) is used for energy regeneration as in other Desulfotomaculum spp. The QmoABC complex contains only the A and B subunit, the C subunit is lacking (Desgi_3699–3700). In all members of the genus Desulfotomaculum the QmoAB is followed by HdrCB (Desgi_3697–3698). This arrangement is identical to that seen in the closely related species “Desulforhudis audaxivator”, Desulfurispora thermophila and the Gram-negative Desulfarculus baarsii and strain NaphS2, which possess a Gram-positive AprBA . Interestingly, the same organization is also found in some phototrophic sulfur-oxidizing bacteria, such as Thiobacillus dentrificans, Thiothrix nivea and Sedimentibacter selenatireducens . Other closely related Gram-positive SRB like Desulfovirgula thermoconiculi and Ammonifex degensii have a complete QmoABC system like all other SRB and the Green Sulfur Bacteria, or have QmoAB linked to a Fe-S oxidoreductase/HdrD as seen in Desulfosporosinus spp. This latter modification is also seen in other Gram-negative SRB, which have a Gram-positive AprBA-like Desulfomonile tiedjei and Syntrophomonas fumaroxidans . It seems that both Desulfotomaculum sp. and Desulfosporosinus have been the source of the entire aps reductase/QmoA complex for members of the Gram-negative Syntrophobacterales . The genomes of Syntrophobacter fumaroxidans and of Desulfovirgula thermoconiculi have two different systems that can be linked to the aps reductase.
D. gibsoniae has six [FeFe] and three [NiFe] hydrogenases, suggesting a lower redundancy in the case of [FeFe] enzymes than other members of the genus. The [FeFe] hydrogenases include one membrane-associated protein (Desgi_0926-0928) that contains a tat motif in the alpha subunit (Desgi_0926), suggesting an extracellular localization; one monomeric hydrogenase (Desgi_0935) encoded close to the membrane-bound enzyme, which suggests the possibility of co-regulation; two copies of trimeric NAD(P)-dependent bifurcating hydrogenases (Desgi_4669-4667 and Desgi_3197-3195); one enzyme (Desgi_0771) that is part of a multi-gene cluster encoding two flavin-dependent oxidoreductases that is also present in other Desulfotomaculum spp., and one HsfB-type hydrogenase (Desgi_3194) encoding a PAS-sensing domain that is likely involved in sensing and regulation, and possibly with the bifurcating Desgi_3195 hydrogenase.
The [NiFe] hydrogenases include one enzyme (Desgi_1398 – 1397) that may also be bound to the membrane by a cytochrome b (Desgi_1402); one simple dimeric enzyme (Desgi_1231-1230); and one trimeric group 3 hydrogenase (Desgi_1166-1164), similar to methyl-viologen reducing hydrogenases from methanogens, and which is encoded next to a HdrA-like protein (Desgi_1163).
A cluster of nitrogenase genes, specifically genes encoding nitrogenase iron protein, nitrogen regulatory protein PII, nitrogenase molybdenum-iron protein alpha chain, nitrogenase molybdenum-iron protein beta chain, nitrogenase molybdenum-iron cofactor biosynthesis protein NifE, nitrogenase molybdenum-iron protein, alpha and beta chains, nitrogenase cofactor biosynthesis protein NifB; ferredoxin, iron only nitrogenase protein AnfO (AnfO_nitrog) (Desgi_2428-2419) were detected within the annotated genome sequence. Thus, D. gibsoniae probably has the capacity for nitrogen fixation. However, the fixation of molecular nitrogen has not been analyzed in this species so far.
The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231, and was also supported by grants CW-TOP 700.55.343, ALW 819.02.014 of the Netherlands Science Foundation (NWO), ERC (project 323009), and BE-Basic (project F07.002.03).
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