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Genome sequence of a dissimilatory Fe(III)-reducing bacterium Geobacter soli type strain GSS01T

Standards in Genomic Sciences volume 10, Article number: 118 (2015) Cite this article

Abstract

Strain GSS01T (=KCTC 4545=MCCC 1 K00269) is the type strain of the species Geobacter soli. G. soli strain GSS01T is of interest due to its ability to reduce insoluble Fe(III) oxides with a wide range of electron donors. Here we describe some key features of this strain, together with the whole genome sequence and annotation. The genome of size 3,657,100 bp contains 3229 protein-coding and 54 RNA genes, including 2 16S rRNA genes. The genome of strain GSS01Tcontains 76 predicted cytochrome genes, 24 pilus assembly protein genes and several other genes, which were proposed to be related to the reduction of insoluble Fe(III) oxides. The genes associated with the electron donors and acceptors of strain GSS01T were predicted in the genome. Information gained from its sequence will be relevant to the future elucidation of extracellular electron transfer mechanism during the reduction of Fe(III) oxides.

Introduction

Geobacter is the type genus of the family Geobacteraceae in the order Desulfuromonadales within the class Deltaproteobacteria [1]. It currently contains 19 validly named species and 2 subspecies isolated from various environments, mostly subsurface anoxic environments. Members of the genus Geobacter are anaerobic, Gram-negative and rod-shaped bacteria. The Geobacter species have the ability to effectively transfer electrons directly onto insoluble extracellular metal (iron) oxides, and thus commonly, are the most abundant microorganisms in anaerobic soils and sediments where metal reduction is an important process [2].

Geobacter soli strain GSS01T (=KCTC 4545=MCCC 1 K00269), is the type strain of the species Geobacter soli [3]. It was originally isolated from soil of an underground ancient forest in Longfu Town, Sihui City, Guangdong Province, China (23o 22′ N 112o 42′ E). Within the genus Geobacter , G. soli has been proposed to form a subclade together with G. sulfurreducens PCA, demonstrating 98.3 % similarity between the 16S rRNA gene sequences [3]. Here, we summarize the physiological features together with the whole genome sequence, annotation and data analysis of G. soli strain GSS01T.

Organism information

Classification and features

Based on the 16S rRNA gene phylogeny and phenotypic characteristics, strain GSS01T was classified as a member of the genus Geobacter , showing the highest similarity to G. anodireducens SD-1T (99.8 %) among all the type strains of the genus Geobacter . G. anodireducens was a new species which was established at almost the same time with G. soli [4], and therefore, no comparison was made between strains GSS01T and SD-1T under the same conditions. The high 16S rRNA gene sequences similarity of 99.8 % between these two species indicates a possibility that G. soli is a heterotypic synonym of G. anodireducens . A 16S rRNA gene-based phylogenetic tree reconstructed using the neighbor-joining method (Fig. 1) shows the phylogenetic neighborhood of G. soli .Within the genus Geobacter , G. soli forms a distinct subclade together with G. anodireducens , G. sulfurreducens subsp. sulfurreducens and G. sulfurreducens subsp. ethanolicus .

Fig. 1
figure 1

Phylogenetic tree based on 16S rRNA gene sequences showing the position of G. soli GSS01T relative to the type strains of other species within the genus Geobacter. The strains and their corresponding GenBank accession numbers of 16S rRNA genes were indicated in parentheses. The sequences were aligned using Clustal W and theneighbor-joining tree was constructed based on kimura 2-paramenter distance model by using MEGA 6 [35]. Bootstrap values above 60 % were shown obtained from 1000 bootstrapreplications. Bar, 0.01 substitutions per nucleotide position. Desulfuromusa kysingii DSM7343 (X79414) was used as an outgroup

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Geobacter soli GSS01T is anaerobic, Gram-stain-negative, motile, rod-shaped (1.0–1.7 μm in length and 0.5 μm in width) and produces monolateral flagella when grown with acetate and Fe(III) citrate (Fig. 2). Growth occurs at 16–40 °C with optimal growth at 30 °C (Table 1). With acetate as the electron donor, ferrihydrite, Fe(III) citrate, Mn (IV), sulfur and 2, 6-anthraquinone-disulphonate can be utilized as electron acceptors. With ferrihydrite as the electron acceptor, acetate, ethanol, glucose, butyrate, pyruvate, benzoate, benzaldehyde, m-cresol and phenol can be utilized as electron donors.

Fig. 2
figure 2

Transmission electron microscopy of strain GSS01T. Scale bar corresponds to 500 nm

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Table 1 Classification and general features of G. soli GSS01T according to the MIGS recommendations [36]
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Genome sequencing information

Genome project history

Geobacter soli GSS01T was selected for genome sequencing based on its phylogenetic position and its ability to reduce insoluble Fe(III) oxides with a wide range of electron donors. The genome sequence was deposited at DDBJ/EMBL/GenBank under the accession JXBL00000000. The version described in this paper is version JXBL01000000. A summary of the project and the Minimum Information about a Genome Sequence were shown in Table 2 and Additional file 1: Table S1.

Table 2 Project information
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Growth conditions and genomic DNA preparation

Geobacter soli strain GSS01T was anaerobically cultivated in a mineral salts medium [MSM, containing (L−1) 0.6 g NaH2PO4, 0.25 g NH4Cl, 0.1 g KCl, 2.5 g NaHCO3, 10.0 ml vitamin stock solution and 10.0 ml mineral stock solution [5], pH 7.2] supplemented with 50 mM Fe(III) citrate and 10 mM acetate as the electron acceptor and donor, respectively. Total genomic DNA was extracted using a DNA extraction kit (Aidlab). The quality and quantity of the genomic DNA was determined by 0.6 % agarose gel electrophoresis with λ-Hind III digest DNA marker and by a Qubit fluorometer (Invitrogen, CA, USA) with Qubit dsDNA BR Assay kit. About 50.22 μg DNA with a concentration of 91.3 ng/μl was obtained.

Genome sequencing and assembly

The genome of strain GSS01T was sequenced at the BGI in Shenzhen using the HiSeq2000 system (Illumina, USA). Two libraries with insert size 463 bp and 6712 bp were constructed and a total of 461 Mb and 232 Mb raw data were produced before filtering, respectively. After removing the adapter, duplicated reads and short inserts from the data of large library, there remained 401 Mb and 202 Mb clean data for assembling, respectively. Then these sequences were assembled into 15 contigs using the SOAPdenovo 2.04 [6] with K setting at 83.

Genome annotation

Whole genomic tRNA were identified using tRNAscan (version 1.23) [7] with the bacterial model, rRNAs were found by rRNAmmer (version 1.2) [8], and sRNA were predicted using Infernal software and the Rfam database (version 10.1) [9]. The genes in the assembled genome were identified using Glimmer (version 3.02) [10]. The predicted ORFs were translated and used to search KEGG (version: 59), COG (version: 20090331), SwissPort (version: 201206), NR (version: 20121005) and GO (version: 1.419) databases. These data sources were combined to assert a product description for each predicted protein. Genes with signal peptides and transmembrane helices were predicted using SignalP server v.4.1 [11] and TMHMM server v.2.0 [12], respectively.

Genome properties

The genome comprised a circular chromosome with a length of 3,657,100 bp with a GC content of 61.76 % (Fig. 3 and Table 3). It was assembled into 15 contigs. A total of 3312 genes were predicted, including 3229 protein-coding genes and 54 RNA genes (48 tRNA genes and two copies of 16S-23S-5S rRNA gene operons). Of the protein-coding genes, 1727 were assigned to COG functional categories. The detailed properties and the statistics of the genome were presented in Table 3. The distribution of genes into COG functional categories was summarized in Fig. 3 and Table 4. The nine Geobacter species genomes (including G. soli ) of characterized isolates were compared in Table 5.

Fig. 3
figure 3

Circular map of the chromosome of G. soli GSS01T. Labeling from the outside to the inside circle: ORFs on the forward strand (colored by COG categories), ORFs on the reverse strand (colored by COG categories), RNA genes, G+C content (peaks out/inside the circle indicate values higher or lower than the average G+C content, respectively) and GC skew

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Table 3 Genome statistics of G. soli strain GSS01T
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Table 4 Number of genes associated with the 25 general COG functional categories
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Table 5 Genome statistics comparison among characterized Geobacter speciesa
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Insights from the genome sequence

Genes associated with insoluble Fe(III) oxide reduction

The ability of Geobacter to reduce insoluble Fe(III) oxides is presumably due to the presence of a vast network of c-type cytochromes that transfer the electrons out of the inner membrane, through the periplasm and outer membrane to Fe(III) oxides [13, 14]. Previous reports revealed that 38 % of the c-type cytochrome proteins encoded in the genome of G. sulfurreducens were predicted to involve in the extracellular electron transfer during the reduction of insoluble Fe(III) oxides, which emphasized the importance of the c-type chrochromes for extracellular electron transfer [13]. Since the c-type cytochromes are not well conserved among Geobacter species [15], it is valuable to investigate the cytochrome content of different Geobacter species.

Proteins were considered as c-type cytochromes if their sequence contained at least one CXXCH motif for covalent heme binding (where X can be anything except one of [CFHPW]) [16]. The analysis of the genome of strain GSS01T showed that 104 open reading frames (ORFs) in the genome contained at least one occurrence of the motif indicating that these may be cytochromes. Since this definition of cytochrome was minimal, a more stringent definition was created using sequence profiles described in the protein database InterPro as c-type cytochromes. Proteins were considered to be c-type cytochromes if their sequence contained at least one profile match in the InterPro database and at least one CXXCH motif. Results showed that genome of strain GSS01T contained 76 cytochromes, and 82 % of the cytochromes contain more than one heme motif –with 7.6 hemes per cytochrome on average (Table 6). These results were in accordance with the reported data of other six Geobacter genomes [15].

Table 6 Description of the predicted cytochrome C proteins
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Studies with G. sulfurreducens have confirmed that the pili of G. sulfurreducens are electrically conductive and, thus, have been proposed to serve as an electronic conduit or ‘nanowire’ between the cell and the insoluble Fe(III) oxides [17]. The pili of G. sulfurreducens are an assembly of a pilin subunit with the conserved N-terminal sequence of bacterial type Iva pillins [17]. The genome sequence of strain GSS01T contained 24 ORFs predicted to code for pilus assembly proteins (Table 7). One of them (SE37_07695) contains the conserved amino-terminal amino acid characteristic of type IVa pilins [18], and shares 85 % similarity with the pilin or PilA peptide of G. sulfurreducens (Gsu1496). Similar to the PilA sequence of G. sulfurreducens and other Geobacter memebers, the predicted length of SE37_07695 (75 amino acids) was considerably shorter than other bacterial pilins [17]. The N-terminal region of SE37_07695 was conserved with those of other reported PilA sequences (Additional file 2: Figure S1) and SE37_07695 contained hydrophobic amino acids (51 amino acids) predicted to form an α-helix using PredictProtein (https://www.predictprotein.org/). This α-helix has been proposed to mediate pilin-pilin interactions during assembly to form a hydrophobic filament core [19]. As observed in the pilin of G. sulfurreducens [17], SE37_07695 contained 6 aromatic amino acids. Five of these aromatic residues are required for pilus conductivity [20]. Besides pilA, almost all genes attributed to pilus biogenesis in G. soli have orthologs in G. sulfurreducens , and the homologues of genes for the formation and assembly of pili are upstream of the G. soli pilA gene, in a conserved genetic arrangement similar to that of the pili genes in G. sulfurreducens [17].

Table 7 Description of pillus assembly protein
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Another gene encoding putative menaquinol oxidoreductase (SE37_00765) that might be involved in the reduction of Fe(III) oxides revealed 86 % similarity to the menaquinol oxidoreducatase complex Cbc5 of G. sulfurreducens . The putative complex Cbc5 was an essential protein for reduction of insoluble Fe(III) oxides in both G. sulfurreducens and G. uraniireducens [13]. In addition, the existence of a number of chemotaxis proteins (count 85) and flagella proteins (count 42) in the genome of strain GSS01T indicated the possibility of accessing insoluble Fe(III) oxides by chemotaxis which was only reported in G. metallireducens [21]. Chemotaxis, mainly depends on motility by flagella, is beneficial for Fe(III) oxide reduction [22], and deletion of the flagellin protein-encoding gene fliC resulted in the loss of ability to reduce insoluble Fe(III) oxides in a G. metallireducens strain [23].

Reduction of other electron acceptors

G. sulfurreducens is capable of oxygen respiration [24] using a cytochrome caa 3 oxidase complex (coxACDB genes) [25], which is also found in G. soli GSS01T (SE37_15290, SE37_15295, SE37_15300, SE37_15305, SE37_15310 and SE37_15315). In addition, the G. soli genome contains a pair of genes encoding cytochrome bd quinol oxidases (SE37_06965 and SE37_06970), which is closely related to its counterparts in G. sulfurreducens . The presence of these proteins indicates that strain GSS01T may grow with oxygen as a terminal electron acceptor. To detoxify reactive oxygen species (ROS) that produced from the oxygen respiration, G. soli possesses a desulfoferrodoxin (SE37_01515), a superoxide dismutase (SE37_09185), a catalase (SE37_11355), 2 peroxiredoxins (SE37_10345 and SE37_14390), 3 rubrerythrins (SE37_02245, SE37_11375 and SE37_11415), and 5 peroxidases (SE37_00200, SE37_10685, SE37_11370, SE37_13285 and SE37_16060), which were also present in G. sulfurreducens . Overall, the genome annotation indicates that, strain GSS01T has evolved to cope with many kinds of ROS to survive oxidative stress, which can ensure cells survive in oxic environments.

Sulfate and nitrate are common electron acceptors in the anaerobic bacteria. G. soli possesses the essential proteins in complete pathway of assimilatory sulfate reduction, including sulfate transporter (SE37_02365, SE37_04150, SE37_08380, SE37_08385 and SE37_08390 and SE37_08640), sulfate adenylyltransferase (SE37_06140), adenylylsulfate reductase (SE37_06145) and sulfite reductase (SE37_08370, SE37_13370 and SE37_15590). Nitrate can be reduced by G. metallireducens but cannot be utilized by G. sulfurreducens [26]. Like G. sulfurreducens , G. soli contains two putative copies of periplasmic nitrite reductases: the first, NfrA (SE37_12935=GSU3154; SE37_16085 = GSU0357), is responsible for the reduction of nitrite to ammonia; the second, NrfH (SE37_12940 = GSU3155), is the small subunit whose likely role is to mediate between the quinone pool and the nitrite reductase. The nitrite reductase (NADH) small subunit, NirD (SE37_02720 = GSU2527) is also found. The presence of these ORFs and the absence of the nitrate reductase indicate the possibility that nitrite can be utilized as an electron acceptor but nitrate can be not. In addition, the putative nitric-oxide reductase NorB (SE37_00345) and NorC (SE37_00350) in G. soli genome, which may participate in reducing nitric oxide to nitrous oxide, are absent in G. sulfurreducens . This foundation indicates that the nitrite metabolism in G. soli may be more complex than that in G. sulfurreducens .

Metabolism of electron donors

Glucose cannot be utilized by most members in the genus Geobacter . Although a complete pathway for glycolysis could be reconstructed, G. sulfurreducens cannot grow with glucose as an electron donor due to the absence of valid sugar transporter in the genome of G. sulfurreducens [27]. To the best of our knowledge, G. bemidjiensis was the first Geobacter species which can utilize glucose as it possessed a unique glucose/galactose transporter (gluP Gbem_3671) belonging to the MFS superfamily [25]. The MFS superfamily is one of the two largest families of membrane transporters, which has a diversity of substrates including simple sugars [28]. In the genome of strain GSS01T, besides a complete glycolysis pathway, 8 MFS transporters were found, 7 of which have orthologs in G. sulfurreducens and 1 is unique in G. soli (SE37_04190, 76 % similarity to that of Thauera aminoaromatica ). Strain GSS01T was able to grow with glucose as electron donor using Fe(III) citrate as the terminal electron acceptor, and this ability may be attributed to the presence of the unique MFS transporter in G. soli genome.

Acetate is expected to be the key electron donor supporting Fe(III) reduction in the Geobacter species. Like G. sulfurreducens , G. soli utilize acetate by two reversible pathways, indicating that acetate may be inefficiently utilized at low concentrations [29]. The first pathway of acetate activation occurs through succinyl-CoA:acetate CoA-transferases (SE37_13685, SE37_00360, and SE37_11235) that convert succinyl-CoA to succinate during oxidation of acetate by the tricarboxylic acid (TCA) cycle [30]. Among the three enzymes, SE37_13685 and SE37_00360 have orthologs in G. sulfurreducens , and SE37_11235 is 83 % identical to Gbem_2843 in G. bemidjiensis . The second pathway consists of two steps: acetate kinases (SE37_01820 and SE37_14395) convert acetate to acetyl-phosphate, and phosphate acetyltransferase (SE37_01825) converts acetyl-phosphte to acetyl-CoA [30].

Strain GSS01T can grow with pyruvate as an electron donor. The interconvert pyruvate and acetyl-CoA is the central reaction during the pyruvate metabolism. Like other Geobacteraceae [25, 30], G. soli possesses two sets of genes encoding pyruvate dehydrogenase complexes (SE37_03080, SE37_02045, SE37_02040, and SE37_03100; SE37_03105 and SE37_02035) to irreversibly convert pyruvate to acetyl-CoA. The reverse reaction in G. soli from acetyl-CoA is attributed to a homodimeric pyruvate-ferredoxin/flavodoxin oxidoreductase (SE37_14040). In addition to pyruvate, ethanol is another electron donor that strain GSS01T can use but G. sulfurreducens cannot. There are two alcohol dehydrogenases (SE37_00690 and SE37_01915) predicted in G. soli genome, in which only SE37_00690 has homolog in G. sulfurreducens (GSU0573) and SE37_01915 that unique for G. soli has 76 % similarity to that in Vibrio parahaemolyticus .

Hydrogen is an electron donor utilized by some Geobacter such as G. sulfurreducens . In the G. soli genome, there are 27 ORFs for hydrogenases, including the orthologs of three large and small subunit [NiFe] hydrogenases (SE37_13920=GSU0122, SE37_13915=GSU0123, SE37_10910=GSU0785, SE37_10925=GSU0782, SE37_03185=GSU2419, and SE37_03190=GSU2418) and two hydrogenase complexes (first complex: SE37_01595 = GSU0739, SE37_01600=GSU0740, SE37_01605=GSU0741, SE37_01610=GSU0742, SE37_01615=GSU0743, SE37_01620 = GSU0745 and possibly SE37_01575=GSU0734; second complex: SE37_01780=GSU2718, SE37_01775=GSU2719, SE37_01770=GSU2720, SE37_01765=GSU2721, SE37_01760=GSU2722) that predicted to participate the hydrogen cycling [31]. In addition, at least two hydrogenases (SE37_02470 and SE37_02475) in G. soli genome have no orthologs in G. sulfurreducens . This result indicates that G. soli may utilize hydrogen as sole electron donor.

Aromatic compounds represent the second most abundant class of natural carbon compounds and many aromatic compounds are major environmental pollutants [32]. Some Geobacter species especially G. metallireducens have the ability to degrade aromatic compounds [33, 34]. Although there is no complete aromatic compound pathway in the genome of G. soli , some genes that may be involved in aromatic compounds degradation are found. For example, 3-hydroxybutyrul-CoA dehydrogenase (SE37_11190, 86 % similarity to Gmet_1717 in G. metallireducens ), acetyl-CoA acetyltransferase (SE37_11195, 83 % similarity to Gmet_1719 in G. metallireducens ) , thiolase (SE37_13640), and tautomerase (SE37_07305) are predicted to be involved in the benzoate degradation; one 4Fe-4S ferredoxin (SE37_08830) and six hydrogenase (SE37_10910, SE37_13915, SE37_13920, SE37_10925, SE37_02470 and SE37_02475) are predicted to be involved in nitrotoluene degradation, among which SE37_02470 and SE37_02475 have no ortholog in G. sulfurreducens ; CoA-transferase (SE37_11150, 85 % similarity to that of G. metallireducens ) and glutaconate CoA-transferase (SE37_11145, 90 % similarity to Gmet_1708 in G. metallireducens ) may be involved in styrene degradation, and these enzymes have no orthologs in G. sulfurreducens . In addition, other enzymes of acyl-CoA metabolism are predicted from the genome of G. soli : acyl-CoA dehydrogenase (SE37_11155, 80 % similarity to Gmet_1710 in G. metallireducens ; SE37_11180, 86 % similarity to that of Geoalkalibacter subterraneus ), succinyl-CoA:acetate CoA-transferases (SE37_00360; SE37_11235, 83 % similarity to Gbem_2843 in G. bemidjiensis ; SE37_13685), acyl-CoA thioesterases (SE37_09325, SE37_09950, SE37_10860, SE37_14445 and SE37_15385), enoyl-CoA hydratases (SE37_15375; SE37_11185, 81 % similarity to Gmet_1716 in G. metallireducens ), phenylacetate-CoA ligase (SE37_04405, SE37_06045 and SE37_06085) and acyl-CoA synthetase (SE37_06810). The ability to utilize aromatic compounds and other carbon sources may be due to stepwise breakdown of multicarbon organic acids to simpler compounds by these enzymes [29].

Conclusions

Geobacter soli type strain GSS01T, isolated from China, can reduce insoluble Fe(III) oxides, such as ferrihydrite, with a variety of electron donors under anaerobic conditions [3]. The insight to the whole genome sequence of strain GSS01T was made based on its ability to reduce electron acceptors with various electron donors. The investigation, especially analysis of the electron transport genes, will be helpful for revealing the mechanism of the extracellular electron transfer of strain GSS01T, and further study of the gene-coding sequence may consequently enhance the understanding of the Fe(III) oxides reduction of Geobacter genus and even microbial community in anaerobic soils and sediments.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (41203078 and 41301257), the Science and Technology Planning Project of Guangdong Province (2013B060400042), and the Industry-University-Research Project of Guangdong Ministry of Education, China (2013B090500017).

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Authors and Affiliations

  1. Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China

    Guiqin Yang

  2. Guangdong Key Laboratory of Agricultural Environment Pollution Integrated Control, Guangdong Institute of Eco-Environmental and Soil Sciences, Guangzhou, 510650, China

    Guiqin Yang, Shanshan Chen & Shungui Zhou

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Guiqin Yang

  4. BGI-Shenzhen, Main Building 11/F, Beishan Industrial Zone, Yantian District, Shenzhen, 518083, China

    Yongfeng Liu

Authors
  1. Guiqin Yang
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  2. Shanshan Chen
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Corresponding author

Correspondence to Shungui Zhou.

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Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

G.Y. prepared the genomic DNA, designed the study, performed the statistical analysis and drafted the manuscript. S.C. participated in the sequence alignment and helped to draft the manuscript. S.Z. participated in the design of the study and helped to revise the manuscript. Y.L. did the de novo assembly of the unmapped raw reads. All authors read and approved the final manuscript.

Additional files

Additional file 1: Table S1.

Associated MIGS record. (PDF 191 kb)

Additional file 2:

Amino acid sequence alignment of pilin domain protein SE37_07695 from Geobacter soli GSS01 and those from other bacteria. Amino acid sequence alignments were generated using the Clustal X (1.8). (PDF 40 kb)

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Yang, G., Chen, S., Zhou, S. et al. Genome sequence of a dissimilatory Fe(III)-reducing bacterium Geobacter soli type strain GSS01T . Stand in Genomic Sci 10, 118 (2015). https://doi.org/10.1186/s40793-015-0117-7

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Keywords

Environmental Microbiome

ISSN: 2524-6372