Bacterial lifestyle in a deep-sea hydrothermal vent chimney revealed by the genome sequence of the thermophilic bacterium Deferribacter desulfuricans SSM1

Abstract

The complete genome sequence of the thermophilic sulphur-reducing bacterium, Deferribacter desulfuricans SMM1, isolated from a hydrothermal vent chimney has been determined. The genome comprises a single circular chromosome of 2,234,389 bp and a megaplasmid of 308,544 bp. Many genes encoded in the genome are most similar to the genes of sulphur- or sulphate-reducing bacterial species within Deltaproteobacteria. The reconstructed central metabolisms showed a heterotrophic lifestyle primarily driven by C1 to C3 organics, e.g. formate, acetate, and pyruvate, and also suggested that the inability of autotrophy via a reductive tricarboxylic acid cycle may be due to the lack of ATP-dependent citrate lyase. In addition, the genome encodes numerous genes for chemoreceptors, chemotaxis-like systems, and signal transduction machineries. These signalling networks may be linked to this bacterium's versatile energy metabolisms and may provide ecophysiological advantages for D. desulfuricans SSM1 thriving in the physically and chemically fluctuating environments near hydrothermal vents. This is the first genome sequence from the phylum Deferribacteres.

Figure 1

Circular representation of the D. desulfuricans SSM1 genome. (A) Chromosome. (B) Megaplasmid pDF308. From the inside, the first and second circles show the GC skew (values greater than or less than zero are indicated in green and pink, respectively) and the G + C percent content (values greater or smaller than the average percentage in the overall chromosome or plasmid are shown in blue and sky blue, respectively) in a 10-kb window with 100-bp step, respectively. The third and fourth circles show the presence of RNAs (rRNA, tRNA, and small RNA genes); CDSs aligned in the clockwise and counterclockwise directions are indicated in the upper and lower sides of the circle, respectively. Different colours indicate different functional categories: red for information storage and processing; green for metabolism; blue for cellular processes and signalling; grey for poorly characterized function; and purple for RNA genes. The outermost circle shows the location of genomic islands (red) and CRISPR/Cas systems (blue). The ‘0’ marked on the outmost circles corresponds to the putative replication origin, and the putative replication termination site of the chromosome is at 1.23 Mb.

Figure 2

Ordination plot of bacterial genomes using NMDS. (A) Analysis with 50 species belonging to 12 phyla and 5 classes, and D. desulfuricans SSM1. (B) Analysis with six species within Deltaproteobacteria and D. desulfuricans SSM1. Distances were calculated from gene profiles based on COG families. The abbreviation corresponding to the KEGG organism code is used as the label for the species name (detailed explanations are described in Supplementary Table S1). The labels are colour-coded according to their taxonomic groups (phylum/class): red, D. desulfuricans SSM1 (def); orange, Deltaproteobacteria; yellow, Epsilonproteobacteria; blue, other Proteobacteria; purple, Firmicutes; green, Chlorobi; black, Aquificae, Thermotogae, and Deinococcus-Thermus; and grey, other bacteria.

Figure 3

Central metabolism based on potential growth substrates and metabolic capacities reconstructed from the D. desulfuricans genome. This figure displays the flow of carbon in the metabolism of various organic acids (acetate, propionate, butyrate, lactate, and glycerol) predicted from the genome information of D. desulfuricans SSM1. The reversible and irreversible reactions catalysed by enzymes are indicated with both and single arrowhead, respectively. POR, pyruvate ferredoxin oxidoreductase; PFL, pyruvate formate-lyase; Pyc, pyruvate carboxylase; Pck, phosphoenolpyruvate carboxykinase; PykA, pyruvate kinase; Ppd, pyruvate phosphate dikinase; MaeB, malate dehydrogenase (oxaloacetate-decarboxylating); Mdh, malate dehydrogenase; SucCD, succinyl-CoA synthase; Sdh, succinate dehydrogenase; OOR, 2-oxogultarate ferredoxin oxidoreductase; Fba, fructose-bisphosphatase; Pfk, 6-phosphofructokinase; Acs, acetyl-CoA synthetase; Ack, acetate kinase; Pta, phosphate acetyltransferase; AOR, aldehyde ferredoxin oxidoreductase; GlpK, glycerol kinase; GlpD, glycerol-3-phosphate dehydrogenase; Thl, acetoacetyl-CoA thiolase; Hbd, 3-hydroxybutyryl-CoA dehydrogenase; Crt, 3-hydroxybutyryl-CoA dehydratase (crotonase); Bcd, butyryl-CoA dehydrogenase; Ptb, phosphate butyryltransferase; Buk, butyrate kinase; Rnf, Rnf-type ion-translocating electron transport complex; Etf, electron transfer flavoprotein complex; PccAB, propionyl-CoA carboxylase; MutAB, methylmalonyl-CoA mutase; 2Pi, diphosphate; and Fdox/Fdred, ferredoxin, oxidized and reduced forms respectively.

Figure 4

Genome-based models for the energy-conserving electron-transport pathways of D. desulfuricans SSM1. Reducing power acquired by catabolic metabolism (NADH, succinate, and sn-glycerol-3-phosphate) or by oxidation of hydrogen and/or formate is used to reduce sulphur compounds and nitrate, and potentially iron ions via the quinol pool for energy conservation or dissipation. Membrane-binding components are indicated with cylinders or cones, where the upper and the lower reactions are catalysed on the periplasmic side and the cytoplasmic side, respectively. Periplasmic components are indicated with ellipsoids or spheres. Hyd, membrane-binding NiFe-hydrogenase; Nar, respiratory membrane-bound nitrate reductase; Nap, periplasmic nitrate reductase; Psr, polysulphide reductase; Phs, thiosulphate reductase; Ttr, tetrathionate reductase; Fdh, formate dehydrogenase; Nuo, proton-pumping NADH dehydrogenase; Nqr, sodium-translocating NADH:quinone oxidoreductase; Sdh, succinate dehydrogenase; Cyt bd, cytochrome bd quinol oxidase; Cyt bc, cytochrome bc complex; Glp, sn-glycerol-3-phosphate dehydrogenase; G3P, sn-glycerol-3-phosphate; and DHAP, dihydroxyacetone phosphate.

Figure 5

Gene arrangement of the representative chemotaxis-like gene clusters in the genomes of D. desulfuricans and related bacteria. Six chemotaxis-like gene clusters (che-1 to che-6) identified in the D. desulfuricans genome are compared with those CheA/Y-containing clusters that have been experimentally verified: M. xanthus Frz, P. aeruginosa Wsp, R. centenum Cluster 3, and Synechocystis sp. PCC 6803 Tax2.