1887

Abstract

A novel mesophilic sulfate-reducing bacterium, strain HN2, was isolated from groundwater sampled from the subsurface siliceous mudstone of the Wakkanai Formation located in Horonobe, Hokkaido, Japan. The bacterium was Gram-negative and vibrio-shaped, and its motility was conferred by a single polar flagellum. Cells had desulfoviridin. Catalase and oxidase activities were not detected. It grew in the temperature range of 25–40 °C (optimum, 35 °C) and pH range of 6.3–8.1 (optimum, pH 7.2–7.6). It used sulfate, thiosulfate, dimethyl sulfoxide, anthraquinone-2,6-disulfonate, Fe, and manganese oxide, but not elemental sulfur, nitrite, nitrate, or fumarate as electron acceptors. The strain showed weak growth with sulfite as the electron acceptor. Fermentative growth with pyruvate, lactate and cysteine was observed in the absence of sulfate, but not with malate or fumarate. NaCl was not required, but the strain tolerated up to 40 g l. Strain HN2 did not require vitamins. The major cellular fatty acids were iso-C (23.8 %), C 9 (18.4 %), C (15.0 %), C (14.5 %), and anteiso-C (10.1 %). The major respiratory quinone was menaquinone MK-6(H). The G+C content of the genomic DNA was 56.7 mol%. Based on 16S rRNA gene sequence analysis, the closest phylogenetic relative of strain HN2 is JS1 (97.0 %). Digital DNA–DNA hybridization (dDDH) and average nucleotide identity (ANI) values of the strains HN2 and JS1 were 22.2 and 79.8 %, respectively. Based on the phenotypic and molecular genetic evidence, we propose a novel species, sp. nov. with the type strain HN2 (=DSM 101010=NBRC 112213).

Funding
This study was supported by the:
  • Ministry of Economy, Trade and Industry
    • Principle Award Recipient: NotApplicable
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004683
2021-02-16
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/2/ijsem004683.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004683&mimeType=html&fmt=ahah

References

  1. Ouattara AS, Patel BK, Cayol JL, Cuzin N, Traore AS et al. Isolation and characterization of Desulfovibrio burkinensis sp. nov. from an African ricefield, and phylogeny of Desulfovibrio alcoholivorans. Int J Syst Bacteriol 1999; 49:639–643 [View Article][PubMed]
    [Google Scholar]
  2. Hines ME, Evans RS, Willis SG, Friedman S et al. Molecular phylogenetic and biogeochemical studies of sulfate-reducing bacteria in the rhizosphere of Spartina alterniflora. Appl Environ Microbiol 1999; 65:2209–2216 [View Article][PubMed]
    [Google Scholar]
  3. Sass H, Berchtold M, Branke J, König H, Cypionka H et al. Psychrotolerant sulfate-reducing bacteria from an oxic freshwater sediment, description of Desulfovibrio cuneatus sp. nov. and Desulfovibrio litoralis sp. nov. Syst Appl Microbiol 1998; 21:212–219 [View Article][PubMed]
    [Google Scholar]
  4. Sakaguchi T, Arakaki A, Matsunaga T. Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. Int J Syst Evol Microbiol 2002; 52:215–221 [View Article][PubMed]
    [Google Scholar]
  5. Sass H, Ramamoorthy S, Yarwood C, Langner H, Schumann P et al. Desulfovibrio idahonensis sp. nov., sulfate-reducing bacteria isolated from a metal(loid)-contaminated freshwater sediment. Int J Syst Evol Microbiol 2009; 59:2208–2214 [View Article][PubMed]
    [Google Scholar]
  6. Haouari O, Fardeau M-L, Casalot L, Tholozan J-L, Hamdi M et al. Isolation of sulfate-reducing bacteria from Tunisian marine sediments and description of Desulfovibrio bizertensis sp. nov. Int J Syst Evol Microbiol 2006; 56:2909–2913 [View Article][PubMed]
    [Google Scholar]
  7. Thioye A, Gam ZBA, Mbengue M, Cayol J-L, Joseph-Bartoli M et al. Desulfovibrio senegalensis sp. nov., a mesophilic sulfate reducer isolated from marine sediment. Int J Syst Evol Microbiol 2017; 67:3162–3166 [View Article][PubMed]
    [Google Scholar]
  8. Reichenbecher W, Schink B. Desulfovibrio inopinatus, sp. nov., a new sulfate-reducing bacterium that degrades hydroxyhydroquinone. Arch Microbiol 1997; 168:338–344 [View Article][PubMed]
    [Google Scholar]
  9. Ben Dhia Thabet O, Fardeau M-L, Suarez-Nuñez C, Hamdi M, Thomas P et al. Desulfovibrio marinus sp. nov., a moderately halophilic sulfate-reducing bacterium isolated from marine sediments in Tunisia. Int J Syst Evol Microbiol 2007; 57:2167–2170 [View Article][PubMed]
    [Google Scholar]
  10. Leloup J, Loy A, Knab NJ, Borowski C, Wagner M et al. Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea. Environ Microbiol 2007; 9:131–142 [View Article][PubMed]
    [Google Scholar]
  11. Leloup J, Fossing H, Kohls K, Holmkvist L, Borowski C et al. Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation. Environ Microbiol 2009; 11:1278–1291 [View Article][PubMed]
    [Google Scholar]
  12. Dhillon A, Teske A, Dillon J, Stahl DA, Sogin ML. Molecular characterization of sulfate-reducing bacteria in the Guaymas Basin. Appl Environ Microbiol 2003; 69:2765–2772 [View Article][PubMed]
    [Google Scholar]
  13. Foti M, Sorokin DY, Lomans B, Mussman M, Zacharova EE et al. Diversity, activity, and abundance of sulfate-reducing bacteria in saline and hypersaline soda lakes. Appl Environ Microbiol 2007; 73:2093–2100 [View Article][PubMed]
    [Google Scholar]
  14. Feio MJ, Zinkevich V, Beech IB, Llobet-Brossa E, Eaton P et al. Desulfovibrio alaskensis sp. nov., a sulphate-reducing bacterium from a soured oil reservoir. Int J Syst Evol Microbiol 2004; 54:1747–1752 [View Article][PubMed]
    [Google Scholar]
  15. Magot M, Caumette P, Desperrier JM, Matheron R, Dauga C et al. Desulfovibrio longus sp. nov., a sulfate-reducing bacterium isolated from an oil-producing well. Int J Syst Bacteriol 1992; 42:398–402 [View Article][PubMed]
    [Google Scholar]
  16. Magot M, Basso O, Tardy-Jacquenod C, Caumette P. Desulfovibrio bastinii sp. nov. and Desulfovibrio gracilis sp. nov., moderately halophilic, sulfate-reducing bacteria isolated from deep subsurface oilfield water. Int J Syst Evol Microbiol 2004; 54:1693–1697 [View Article][PubMed]
    [Google Scholar]
  17. Miranda-Tello E, Fardeau M-L, Fernández L, Ramírez F, Cayol J-L et al. Desulfovibrio capillatus sp. nov., a novel sulfate-reducing bacterium isolated from an oil field separator located in the Gulf of Mexico. Anaerobe 2003; 9:97–103 [View Article][PubMed]
    [Google Scholar]
  18. Tardy-Jacquenod C, Magot M, Laigret F, Kaghad M, Patel BK et al. Desulfovibrio gabonensis sp. nov., a new moderately halophilic sulfate-reducing bacterium isolated from an oil pipeline. Int J Syst Bacteriol 1996; 46:710–715 [View Article][PubMed]
    [Google Scholar]
  19. Ben Ali Gam Z, Oueslati R, Abdelkafi S, Casalot L, Tholozan JL et al. Desulfovibrio tunisiensis sp. nov., a novel weakly halotolerant, sulfate-reducing bacterium isolated from exhaust water of a Tunisian oil refinery. Int J Syst Evol Microbiol 2009; 59:1059–1063 [View Article][PubMed]
    [Google Scholar]
  20. Dang PN, Dang TCH, Lai TH, Stan-Lotter H. Desulfovibrio vietnamensis sp.nov., a halophilic sulfate-reducing bacterium from Vietnamese oil fields. Anaerobe 1996; 2:385–392 [View Article]
    [Google Scholar]
  21. In Widdel F. Microbiology and ecology of sulphate- and sulfur-reducing bacteria. Biology of Anaerobic Microorganisms New York: John Wiley & Sons Inc; 1988 pp 469–585
    [Google Scholar]
  22. Barton LL, Hamilton WA. Sulphate-Reducing Bacteria: Environmental and Engineered Systems Cambridge University Press; 2007
    [Google Scholar]
  23. Parte AC. LPSN - List of Prokaryotic names with standing in nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 2018; 68:1825–1829 [View Article][PubMed]
    [Google Scholar]
  24. Pecheritsyna SA, Rivkina EM, Akimov VN, Shcherbakova VA. Desulfovibrio arcticus sp. nov., a psychrotolerant sulfate-reducing bacterium from a cryopeg. Int J Syst Evol Microbiol 2012; 62:33–37 [View Article][PubMed]
    [Google Scholar]
  25. Sass H, Cypionka H. Isolation of sulfate-reducing bacteria from the terrestrial deep subsurface and description of Desulfovibrio cavernae sp. nov. Syst Appl Microbiol 2004; 27:541–548 [View Article][PubMed]
    [Google Scholar]
  26. Basso O, Caumette P, Magot M. Desulfovibrio putealis sp. nov., a novel sulfate-reducing bacterium isolated from a deep subsurface aquifer. Int J Syst Evol Microbiol 2005; 55:101–104 [View Article][PubMed]
    [Google Scholar]
  27. Redburn AC, Patel BK. Desulfovibrio longreachii sp. nov., a sulfate-reducing bacterium isolated from the great Artesian Basin of Australia. FEMS Microbiol Lett 1994; 115:33–38 [View Article][PubMed]
    [Google Scholar]
  28. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 1998; 95:6578–6583 [View Article][PubMed]
    [Google Scholar]
  29. Wilkins MJ, Daly RA, Mouser PJ, Trexler R, Sharma S, Wrighton K et al. Trends and future challenges in sampling the deep terrestrial biosphere. Front Microbiol 2014; 5:481 [View Article][PubMed]
    [Google Scholar]
  30. Wu X, Pedersen K, Edlund J, Eriksson L, Åström M et al. Potential for hydrogen-oxidizing chemolithoautotrophic and diazotrophic populations to initiate biofilm formation in oligotrophic, deep terrestrial subsurface waters. Microbiome 2017; 5:37 [View Article][PubMed]
    [Google Scholar]
  31. Hama K, Kunimaru T, Metcalfe R, Martin AJ. The hydrogeochemistry of argillaceous rock formations at the Horonobe URL site, Japan. Physics and Chemistry of the Earth, Parts A/B/C 2007; 32:170–180 [View Article]
    [Google Scholar]
  32. Shimizu S, Akiyama M, Ishijima Y, Hama K, Kunimaru T et al. Molecular characterization of microbial communities in fault-bordered aquifers in the Miocene formation of northernmost Japan. Geobiology 2006; 4:203–213 [View Article]
    [Google Scholar]
  33. Hungate RE. A roll-tube method for the cultivation of strict anaerobes. Methods Microbiol 1969; 3B:117–132
    [Google Scholar]
  34. Shimizu S, Upadhye R, Ishijima Y, Naganuma T. Methanosarcina horonobensis sp. nov., a methanogenic archaeon isolated from a deep subsurface Miocene formation. Int J Syst Evol Microbiol 2011; 61:2503–2507 [View Article][PubMed]
    [Google Scholar]
  35. Shimizu S, Ueno A, Tamamura S, Naganuma T, Kaneko K. Methanoculleus horonobensis sp. nov., a methanogenic archaeon isolated from a deep diatomaceous shale formation. Int J Syst Evol Microbiol 2013; 63:4320–4323 [View Article][PubMed]
    [Google Scholar]
  36. Shimizu S, Ueno A, Naganuma T, Kaneko K. Methanosarcina subterranea sp. nov., a methanogenic archaeon isolated from a deep subsurface diatomaceous shale formation. Int J Syst Evol Microbiol 2015; 65:1167–1171 [View Article][PubMed]
    [Google Scholar]
  37. Zinkevich V, Beech IB. Screening of sulfate-reducing bacteria in colonoscopy samples from healthy and colitic human gut mucosa. FEMS Microbiol Ecol 2000; 34:147–155 [View Article][PubMed]
    [Google Scholar]
  38. Ben Ali Gam Z, Thioye A, Cayol JL, Joseph M, Fauque G et al. Characterization of Desulfovibrio salinus sp. nov., a slightly halophilic sulfate-reducing bacterium isolated from a saline lake in Tunisia. Int J Syst Evol Microbiol 2018; 68:715–720 [View Article][PubMed]
    [Google Scholar]
  39. 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]
  40. Kumar S, Stecher G, Tamura K. mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  41. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article][PubMed]
    [Google Scholar]
  42. Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast Distance-Based phylogeny inference program. Mol Biol Evol 2015; 32:2798–2800 [View Article][PubMed]
    [Google Scholar]
  43. Farris JS. Estimating phylogenetic trees from distance matrices. Am Nat 1972; 106:645–668 [View Article]
    [Google Scholar]
  44. Sasi Jyothsna TS, Sasikala C, Ramana CV, Ch R. Desulfovibrio psychrotolerans sp. nov., a psychrotolerant and moderately alkaliphilic sulfate-reducing deltaproteobacterium from the Himalayas. Int J Syst Evol Microbiol 2008; 58:821–825 [View Article][PubMed]
    [Google Scholar]
  45. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article][PubMed]
    [Google Scholar]
  46. Kajitani R, Toshimoto K, Noguchi H, Toyoda A, Ogura Y et al. Efficient de novo assembly of highly heterozygous genomes from whole-genome shotgun short reads. Genome Res 2014; 24:1384–1395 [View Article][PubMed]
    [Google Scholar]
  47. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  48. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  49. Auch AF, von Jan M, Klenk H-P, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2010; 2:117–134 [View Article][PubMed]
    [Google Scholar]
  50. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  51. Kanehisa M, Sato Y, Morishima K, BlastKOALA MK. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article][PubMed]
    [Google Scholar]
  52. Graham ED, Heidelberg JF, Tully BJ. Potential for primary productivity in a globally-distributed bacterial phototroph. Isme J 2018; 12:1861–1866 [View Article][PubMed]
    [Google Scholar]
  53. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
    [Google Scholar]
  54. Postgate JR. The Sulphate-Reducing Bacteria, 2nd ed. Cambridge: Cambridge University Press; 1983
    [Google Scholar]
  55. Loubinoux J, Valente FMA, Pereira IAC, Costa A, Grimont PAD et al. Reclassification of the only species of the genus Desulfomonas, Desulfomonas pigra, as Desulfovibrio piger comb. nov. Int J Syst Evol Microbiol 2002; 52:1305–1308 [View Article][PubMed]
    [Google Scholar]
  56. Bale SJ, Goodman K, Rochelle PA, Marchesi JR, Fry JC et al. Desulfovibrio profundus sp. nov., a novel barophilic sulfate-reducing bacterium from deep sediment layers in the Japan Sea. Int J Syst Bacteriol 1997; 47:515–521 [View Article][PubMed]
    [Google Scholar]
  57. Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V et al. The complete genome sequence of Escherichia coli K-12. Science 1997; 277:1453–1462 [View Article][PubMed]
    [Google Scholar]
  58. Badziong W, Thauer RK, Zeikus JG. Isolation and characterization of Desulfovibrio growing on hydrogen plus sulfate as the sole energy source. Arch Microbiol 1978; 116:41–49 [View Article][PubMed]
    [Google Scholar]
  59. Lovley DR, Roden EE, Phillips EJP, Woodward JC. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar Geol 1993; 113:41–53 [View Article]
    [Google Scholar]
  60. Stucki JW. The quantitative assay of minerals for Fe²+ and Fe³+using 1,10-phenanthroline: II. A photochemical method. Soil Sci Soc Am J 1981; 45:638–641 [View Article]
    [Google Scholar]
  61. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJ, Woodward JC. Humic substances as electron acceptors for microbial respiration. Nature 1996; 382:445–448 [View Article]
    [Google Scholar]
  62. Wolin EA, Wolin MJ, Wolfe RS. Formation of methane by bacterial extracts. J Biol Chem 1963; 238:2882–2886 [View Article][PubMed]
    [Google Scholar]
  63. Hobbie JE, Daley RJ, Jasper S. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 1977; 33:1225–1228 [View Article][PubMed]
    [Google Scholar]
  64. Cord-Ruwisch R. A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 1985; 4:33–36 [View Article]
    [Google Scholar]
  65. Tamamura S, Murakami T, Aramaki N, Ueno A, Tamazawa S et al. The role of meteoric water recharge in stimulating biogenic methane generation: a case study from the Tempoku coal field, Japan. Int J Coal Geol 2019; 202:14–26 [View Article]
    [Google Scholar]
  66. Tamazawa S, Mayumi D, Mochimaru H, Sakata S, Maeda H et al. Petrothermobacter organivorans gen. nov., sp. nov., a thermophilic, strictly anaerobic bacterium of the phylum Deferribacteres isolated from a deep subsurface oil reservoir. Int J Syst Evol Microbiol 2017; 67:3982–3986 [View Article][PubMed]
    [Google Scholar]
  67. Takii S, Hanada S, Hase Y, Tamaki H, Uyeno Y et al. Desulfovibrio marinisediminis sp. nov., a novel sulfate-reducing bacterium isolated from coastal marine sediment via enrichment with Casamino acids. Int J Syst Evol Microbiol 2008; 58:2433–2438 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004683
Loading
/content/journal/ijsem/10.1099/ijsem.0.004683
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error