1887

Abstract

A novel mesophilic, obligately anaerobic, facultatively sulphur-reducing bacterium, designated strain IC12, was isolated from a deep-sea hydrothermal field in the Mid-Okinawa Trough, Japan. The cells were Gram-negative, motile, short rods with a single polar flagellum. The ranges and optima of the growth temperature, NaCl concentration and pH of strain IC12 were 15–40 °C (optimum, 30–35 °C), 10–60 g l (optimum, 20–30 g l) and pH 4.9–6.7 (optimum, pH 5.8), respectively. Yeast extract was utilized as a sole carbon and energy source for fermentative growth. Major fatty acids of strain IC12 were C, C and C ω7. Results of phylogenetic analysis based on 16S rRNA gene sequences indicated that strain IC12 was affiliated to the phylum and was most closely related to VenChi2 (86.5 % sequence similarity). Strain IC12 contained a chromosome of 2.43 Mbp and a large plasmid of 0.30 Mbp. The G+C content of the genomic DNA was 26.4 mol%. The maximum values for average nucleotide identity and DNA–DNA hybridization between strain IC12 and related strains of the phylum were 71.4 and 26.4 %, respectively. Phylogenomic, physiological and chemotaxonomic analyses indicate that strain IC12 represents a novel genus and species within the phylum , for which the name gen. nov., sp. nov. is proposed, with strain IC12 (= DSM 112164=JCM 39166) as the type strain. We also propose the family fam. nov. to accommodate this novel genus.

Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 20H03322)
    • Principle Award Recipient: SatoshiNakagawa
  • Japan Society for the Promotion of Science (Award 16H04843)
    • Principle Award Recipient: SatoshiNakagawa
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2023-08-04
2024-05-08
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References

  1. Gupta RS, Sethi M. Phylogeny and molecular signatures for the phylum Fusobacteria and its distinct subclades. Anaerobe 2014; 28:182–198 [View Article] [PubMed]
    [Google Scholar]
  2. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:005056 [View Article]
    [Google Scholar]
  3. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  4. Verma D, Garg PK, Dubey AK. Insights into the human oral microbiome. Arch Microbiol 2018; 200:525–540 [View Article] [PubMed]
    [Google Scholar]
  5. Moon CD, Young W, Maclean PH, Cookson AL, Bermingham EN. Metagenomic insights into the roles of Proteobacteria in the gastrointestinal microbiomes of healthy dogs and cats. MicrobiologyOpen 2018; 7:e00677 [View Article] [PubMed]
    [Google Scholar]
  6. Gutierrez T, Berry D, Teske A, Aitken MD. Enrichment of Fusobacteria in sea surface oil slicks from the deepwater horizon oil spill. Microorganisms 2016; 4:24 [View Article] [PubMed]
    [Google Scholar]
  7. Liang J-B, Chen Y-Q, Lan C-Y, Tam NFY, Zan Q-J et al. Recovery of novel bacterial diversity from mangrove sediment. Mar Biol 2007; 150:739–747 [View Article]
    [Google Scholar]
  8. Eribe ERK, Olsen I. Leptotrichia species in human infections. Anaerobe 2008; 14:131–137 [View Article] [PubMed]
    [Google Scholar]
  9. Schink B, Pfennig N. Propionigenium modestum gen. nov. sp. nov. a new strictly anaerobic, nonsporing bacterium growing on succinate. Arch Microbiol 1982; 133:209–216 [View Article]
    [Google Scholar]
  10. Eribe ERK, Paster BJ, Caugant DA, Dewhirst FE, Stromberg VK et al. Genetic diversity of Leptotrichia and description of Leptotrichia goodfellowii sp. nov., Leptotrichia hofstadii sp. nov., Leptotrichia shahii sp. nov. and Leptotrichia wadei sp. nov. Int J Syst Evol Microbiol 2004; 54:583–592 [View Article] [PubMed]
    [Google Scholar]
  11. Eisenberg T, Ewers C, Rau J, Akimkin V, Nicklas W. Approved and novel strategies in diagnostics of rat bite fever and other Streptobacillus infections in humans and animals. Virulence 2016; 7:630–648 [View Article] [PubMed]
    [Google Scholar]
  12. Eisenberg T, Heydel C, Prenger-Berninghoff E, Fawzy A, Kling U et al. Streptobacillus canis sp. nov. isolated from a dog. Int J Syst Evol Microbiol 2020; 70:2648–2656 [View Article]
    [Google Scholar]
  13. Volokhov DV, Blom J, Amselle M, Delmonte P, Gao Y et al. Oceanivirga miroungae sp. nov., isolated from oral cavity of northern elephant seal (Mirounga angustirostris). Int J Syst Evol Microbiol 2020; 70:3037–3048 [View Article]
    [Google Scholar]
  14. Eisenberg T, Kämpfer P, Ewers C, Semmler T, Glaeser SP et al. Oceanivirga salmonicida gen. nov., sp. nov., a member of the Leptotrichiaceae isolated from Atlantic salmon (Salmo salar). Int J Syst Evol Microbiol 2016; 66:2429–2437 [View Article] [PubMed]
    [Google Scholar]
  15. Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science 2017; 358:1443–1448 [View Article] [PubMed]
    [Google Scholar]
  16. Finegold SM, Vaisanen M-L, Molitoris DR, Tomzynski TJ, Song Y et al. Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. Syst Appl Microbiol 2003; 26:177–181 [View Article]
    [Google Scholar]
  17. Zhao J-S, Manno D, Hawari J. Psychrilyobacter atlanticus gen. nov., sp. nov., a marine member of the phylum Fusobacteria that produces H2 and degrades nitramine explosives under low temperature conditions. Int J Syst Evol Microbiol 2009; 59:491–497
    [Google Scholar]
  18. Stieb M, Schink B. A new 3-hydroxybutyrate fermenting anaerobe, Ilyobacter polytropus, gen. nov. sp. nov., possessing various fermentation pathways. Arch Microbiol 1984; 140:139–146 [View Article]
    [Google Scholar]
  19. Roalkvam I, Bredy F, Baumberger T, Pedersen R-B, Steen IH. Hypnocyclicus thermotrophus gen. nov., sp. nov. isolated from a microbial mat in a hydrothermal vent field. Int J Syst Evol Microbiol 2015; 65:4521–4525 [View Article] [PubMed]
    [Google Scholar]
  20. Ludwig W, Euzéby J, Whitman WB. Road map of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. In Krieg NR, Staley JT, Brown DR, Hedlund BP, Paster BJ. eds Bergey’s Manual® of Systematic Bacteriology: Volume Four The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes New York, NY: Springer; pp 1–19
    [Google Scholar]
  21. De Witte C, Flahou B, Ducatelle R, Smet A, De Bruyne E et al. Detection, isolation and characterization of Fusobacterium gastrosuis sp. nov. colonizing the stomach of pigs. Syst Appl Microbiol 2017; 40:42–50 [View Article] [PubMed]
    [Google Scholar]
  22. Brune A, Evers S, Kaim G, Ludwig W, Schink B. Ilyobacter insuetus sp. nov., a fermentative bacterium specialized in the degradation of hydroaromatic compounds. Int J Syst Evol Microbiol 2002; 52:429–432 [View Article]
    [Google Scholar]
  23. Janssen PH, Liesack W. Succinate decarboxylation by Propionigenium maris sp. nov., a new anaerobic bacterium from an estuarine sediment. Arch Microbiol 1995; 164:29–35 [View Article] [PubMed]
    [Google Scholar]
  24. Bennett KW, Eley A. Fusobacteria: new taxonomy and related diseases. J Med Microbiol 1993; 39:246–254 [View Article] [PubMed]
    [Google Scholar]
  25. Zhang Z, Fan Z, Yi M, Liu Z, Ke X et al. Characterization of the core gut microbiota of Nile tilapia (Oreochromis niloticus): indication of a putative novel Cetobacterium species and analysis of its potential function on nutrition. Arch Microbiol 2022; 204:690 [View Article]
    [Google Scholar]
  26. Mukherjee A, Rodiles A, Merrifield DL, Chandra G, Ghosh K. Exploring intestinal microbiome composition in three Indian major carps under polyculture system: a high-throughput sequencing based approach. Aquaculture 2020; 524:735206 [View Article]
    [Google Scholar]
  27. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM et al. Evidence for a core gut microbiota in the zebrafish. ISME J 2011; 5:1595–1608 [View Article]
    [Google Scholar]
  28. Janssen PH, Harfoot CG. Ilyobacter delafieldii sp. nov., a metabolically restricted anaerobic bacterium fermenting PHB. Arch Microbiol 1990; 154:253–259 [View Article]
    [Google Scholar]
  29. Schink B. Fermentation of tartrate enantiomers by anaerobic bacteria, and description of two new species of strict anaerobes, Ruminococcus pasteurii and Ilyobacter tartaricus. Arch Microbiol 1984; 139:409–414 [View Article]
    [Google Scholar]
  30. Enomoto M, Nakagawa S, Sawabe T. Microbial communities associated with holothurians: presence of unique bacteria in the coelomic fluid. Microbes Environ 2012; 27:300–305 [View Article] [PubMed]
    [Google Scholar]
  31. Yadav S, Koenen M, Bale N, Sinninghe Damsté JS, Villanueva L. The physiology and metabolic properties of a novel, low-abundance Psychrilyobacter species isolated from the anoxic Black Sea shed light on its ecological role. Environ Microbiol Rep 2021; 13:899–910 [View Article] [PubMed]
    [Google Scholar]
  32. Huber JA, Mark Welch DB, Morrison HG, Huse SM, Neal PR et al. Microbial population structures in the deep marine biosphere. Science 2007; 318:97–100 [View Article] [PubMed]
    [Google Scholar]
  33. Alain K, Zbinden M, Le Bris N, Lesongeur F, Quérellou J et al. Early steps in microbial colonization processes at deep-sea hydrothermal vents. Environ Microbiol 2004; 6:227–241 [View Article] [PubMed]
    [Google Scholar]
  34. Callac N, Rommevaux-Jestin C, Rouxel O, Lesongeur F, Liorzou C et al. Microbial colonization of basaltic glasses in hydrothermal organic-rich sediments at Guaymas Basin. Front Microbiol 2013; 4:250 [View Article] [PubMed]
    [Google Scholar]
  35. Nunoura T, Takaki Y, Kazama H, Hirai M, Ashi J et al. Microbial diversity in deep-sea methane seep sediments presented by SSU rRNA gene tag sequencing. Microbes Environ 2012; 27:382–390 [View Article] [PubMed]
    [Google Scholar]
  36. Durvasula R, Rao DVS. Deep-sea vent extremophiles: cultivation, physiological characteristics, and ecological significance. In Extremophiles CRC Press; 2017
    [Google Scholar]
  37. Takai K, Nakagawa S, Sako Y, Horikoshi K. Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. Int J Syst Evol Microbiol 2003; 53:1947–1954 [View Article] [PubMed]
    [Google Scholar]
  38. Nakagawa S, Takai K, Inagaki F, Horikoshi K, Sako Y. Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the ε-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 2005; 55:925–933 [View Article] [PubMed]
    [Google Scholar]
  39. Nakagawa S, Inagaki F, Takai K, Horikoshi K, Sako Y. Thioreductor micantisoli gen. nov., sp. nov., a novel mesophilic, sulfur-reducing chemolithoautotroph within the ε-Proteobacteria isolated from hydrothermal sediments in the Mid-Okinawa Trough. Int J Syst Evol Microbiol 2005; 55:599–605 [View Article] [PubMed]
    [Google Scholar]
  40. Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J et al. Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol Ecol 2005; 54:141–155 [View Article] [PubMed]
    [Google Scholar]
  41. Watsuji T-O, Nakagawa S, Tsuchida S, Toki T, Hirota A et al. Diversity and function of epibiotic microbial communities on the galatheid crab, Shinkaia crosnieri. Microbes Environ 2010; 25:288–294 [View Article] [PubMed]
    [Google Scholar]
  42. Stetter KO, König H, Stackebrandt E. Pyrodictium gen. nov., a new genus of submarine disc-shaped sulphur reducing Archaebacteria growing optimally at 105°C. Syst Appl Microbiol 1983; 4:535–551 [View Article] [PubMed]
    [Google Scholar]
  43. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS. Methanogens: reevaluation of a unique biological group. Microbiol Rev 1979; 43:260–296 [View Article] [PubMed]
    [Google Scholar]
  44. Baross JA. Isolation, growth, and maintenance of hyperthermophiles. In Archaea, a Laboratory Manual, Thermophiles CSHL Press; 1995 pp 15–23
    [Google Scholar]
  45. Hashimoto Y, Tame A, Sawayama S, Miyazaki J, Takai K et al. Desulfomarina profundi gen. nov., sp. nov., a novel mesophilic, hydrogen-oxidizing, sulphate-reducing chemolithoautotroph isolated from a deep-sea hydrothermal vent chimney. Int J Syst Evol Microbiol 2021; 71:005083 [View Article] [PubMed]
    [Google Scholar]
  46. Porter KG, Feig YS. The use of DAPI for identifying and counting aquatic microflora1. Limnol Oceanogr 1980; 25:943–948 [View Article]
    [Google Scholar]
  47. Kato C, Li L, Tamaoka J, Horikoshi K. Molecular analyses of the sediment of the 11,000-m deep Mariana Trench. Extremophiles 1997; 1:117–123 [View Article] [PubMed]
    [Google Scholar]
  48. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  49. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  50. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  51. Kumar S, Stecher G, Li M, Knyaz C, Tamura K et al. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
    [Google Scholar]
  52. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article] [PubMed]
    [Google Scholar]
  53. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM et al. Microbial diversity in the deep sea and the underexplored “rare biosphere.”. Proc Natl Acad Sci 2006; 103:12115–12120 [View Article]
    [Google Scholar]
  54. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  55. Schwengers O, Barth P, Falgenhauer L, Hain T, Chakraborty T et al. Platon: identification and characterization of bacterial plasmid contigs in short-read draft assemblies exploiting protein sequence-based replicon distribution scores. Microb Genom 2020; 6:mgen000398 [View Article] [PubMed]
    [Google Scholar]
  56. Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics 2012; 28:464–469 [View Article]
    [Google Scholar]
  57. Tanizawa Y, Fujisawa T, Nakamura Y. DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 2018; 34:1037–1039 [View Article] [PubMed]
    [Google Scholar]
  58. Sikorski J, Chertkov O, Lapidus A, Nolan M, Lucas S et al. Complete genome sequence of Ilyobacter polytropus type strain (CuHbu1T). Stand Genomic Sci 2010; 3:304–314 [View Article]
    [Google Scholar]
  59. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  60. Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M et al. KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics 2019; 362251–2252 [View Article]
    [Google Scholar]
  61. Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA et al. Pfam: the protein families database in 2021. Nucleic Acids Res 2021; 49:D412–D419 [View Article] [PubMed]
    [Google Scholar]
  62. Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 2020; 48:D265–D268 [View Article]
    [Google Scholar]
  63. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
    [Google Scholar]
  64. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993; 10:512–526 [View Article] [PubMed]
    [Google Scholar]
  65. Ankenbrand MJ, Keller A. bcgTree: automatized phylogenetic tree building from bacterial core genomes. Genome 2016; 59:783–791 [View Article] [PubMed]
    [Google Scholar]
  66. Dombrowski N, Seitz KW, Teske AP, Baker BJ. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome 2017; 5:106 [View Article] [PubMed]
    [Google Scholar]
  67. Søndergaard D, Pedersen CNS, Greening C. HydDB: A web tool for hydrogenase classification and analysis. Sci Rep 2016; 6:34212 [View Article] [PubMed]
    [Google Scholar]
  68. Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM et al. [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta 2015; 1853:1350–1369 [View Article] [PubMed]
    [Google Scholar]
  69. Calusinska M, Joris B, Wilmotte A. Genetic diversity and amplification of different clostridial [FeFe] hydrogenases by group-specific degenerate primers. Lett Appl Microbiol 2011; 53:473–480 [View Article] [PubMed]
    [Google Scholar]
  70. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  71. Suzuki D, Ueki A, Amaishi A, Ueki K. Desulfobulbus japonicus sp. nov., a novel gram-negative propionate-oxidizing, sulfate-reducing bacterium isolated from an estuarine sediment in Japan. Int J Syst Evol Microbiol 2007; 57:849–855 [View Article] [PubMed]
    [Google Scholar]
  72. Nagata R, Takaki Y, Tame A, Nunoura T, Muto H et al. Lebetimonas natsushimae sp. nov., a novel strictly anaerobic, moderately thermophilic chemoautotroph isolated from a deep-sea hydrothermal vent polychaete nest in the Mid-Okinawa Trough. Syst Appl Microbiol 2017; 40:352–356 [View Article] [PubMed]
    [Google Scholar]
  73. Ramotar K, Conly JM, Chubb H, Louie TJ. Production of menaquinones by intestinal anaerobes. J Infect Dis 1984; 150:213–218 [View Article] [PubMed]
    [Google Scholar]
  74. Collins MD, Shah HN. Reclassification of Bacteroides termitidis Sebald (Holdeman and Moore) in a new genus Sebaldella, as Sebaldella termitidis comb. nov. Int J Syst Bacteriol 1986; 36:349–350 [View Article]
    [Google Scholar]
  75. Kapatral V, Anderson I, Ivanova N, Reznik G, Los T et al. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 2002; 184:2005–2018 [View Article] [PubMed]
    [Google Scholar]
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