1887

Abstract

A novel mesophilic, anaerobic, mixotrophic bacterium, with designated strains EPR-M and HR-1, was isolated from a semi-extinct hydrothermal vent at the East Pacific Rise and from an Fe-mat at Lō'ihi Seamount, respectively. The cells were Gram-negative, pleomorphic rods of about 2.0 µm in length and 0.5 µm in width. Strain EPR-M grew between 25 and 45 °C (optimum, 37.5–40 °C), 10 and 50 g l NaCl (optimum, 15–20 g l) and pH 5.5 and 8.6 (optimum, pH 6.4). Strain HR-1 grew between 20 and 45 °C (optimum, 37.5–40 °C), 10 and 50 g l NaCl (optimum, 15–25 g l) and pH 5.5 and 8.6 (optimum, pH 6.4). Shortest generation times with H as the primary electron donor, CO as the carbon source and ferric citrate as terminal electron acceptor were 6.7 and 5.5 h for EPR-M and HR-1, respectively. Fe(OH), MnO, AsO , SO , SeO , SO , S and NO were also used as terminal electron acceptors. Acetate, yeast extract, formate, lactate, tryptone and Casamino acids also served as both electron donors and carbon sources. G+C content of the genomic DNA was 59.4 mol% for strain EPR-M and 59.2 mol% for strain HR-1. Phylogenetic and phylogenomic analyses indicated that both strains were closely related to each other and to , within the class δ- (now within the class ). Based on phylogenetic and phylogenomic analyses in addition to physiological and biochemical characteristics, both strains were found to represent a novel species within the genus , for which the name sp. nov. is proposed. is represented by type strain EPR-M (=JCM 32109=KCTC 15831=ATCC TSD-173) and strain HR-1 (=JCM 32110=KCTC 15832).

Funding
This study was supported by the:
  • NSF Science and Technology Center (C-DEBI) (Award OCE-1431598)
    • Principle Award Recipient: JanAmend
  • Center for Dark Energy Biosphere Investigations (Award OCE-1460892)
    • Principle Award Recipient: JanAmend
  • University of Pennsylvania (Award University of Pennsylvania (Penn) Start-up Funds and Elliman Faculty Fellowship)
    • Principle Award Recipient: IleanaM. Pérez-Rodríguez
  • Center for Dark Energy Biosphere Investigations (Award Postdoctoral Fellowship)
    • Principle Award Recipient: IleanaM. Pérez-Rodríguez
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2021-04-20
2021-05-17
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References

  1. Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P et al. Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol 2020; 70:5972–6016 [CrossRef][PubMed]
    [Google Scholar]
  2. Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S et al. NCBI taxonomy: a comprehensive update on curation, resources and tools. Database 2020; 2020: 01 01 2020 [CrossRef][PubMed]
    [Google Scholar]
  3. Röling WFM. The family Geobacteraceae . In Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F. (editors) The Prokaryotes Berlin, Heidelberg: Springer; 2014 [CrossRef]
    [Google Scholar]
  4. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 1993; 159:336–344 [CrossRef][PubMed]
    [Google Scholar]
  5. Kashefi K, Holmes DE, Baross JA, Lovley DR. Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a novel thermophilic member of the Geobacteraceae from the "Bag City" hydrothermal vent. Appl Environ Microbiol 2003; 69:2985–2993 [CrossRef][PubMed]
    [Google Scholar]
  6. Holmes DE, Nicoll JS, Bond DR, Lovley DR. Potential role of a novel psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl Environ Microbiol 2004; 70:6023–6030 [CrossRef][PubMed]
    [Google Scholar]
  7. Zavarzina DG, Kolganova TV, Bulygina ES, Kostrikina NA, Turova TP et al. Geoalkalibacter ferrihydriticus gen. nov., sp. nov., the first alkaliphilic representative of the family Geobacteraceae, isolated from a soda lake]. Mikrobiologiia 2006; 75:673–682 [CrossRef][PubMed]
    [Google Scholar]
  8. Xu Z, Masuda Y, Itoh H, Ushijima N, Shiratori Y et al. Geomonas oryzae gen. nov., sp. nov., Geomonas edaphica sp. nov., Geomonas ferrireducens sp. nov., Geomonas terrae sp. nov., Four Ferric-Reducing Bacteria Isolated From Paddy Soil, and Reclassification of Three Species of the Genus Geobacter as Members of the Genus Geomonas gen. nov. Front Microbiol 2019; 10:2201 [CrossRef][PubMed]
    [Google Scholar]
  9. Lovley DR, Phillips EJ. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 1988; 54:1472–1480 [CrossRef][PubMed]
    [Google Scholar]
  10. Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF et al. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 1994; 60:3752–3759 [CrossRef][PubMed]
    [Google Scholar]
  11. Nevin KP, Holmes DE, Woodard TL, Hinlein ES, Ostendorf DW et al. Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int J Syst Evol Microbiol 2005; 55:1667–1674 [CrossRef][PubMed]
    [Google Scholar]
  12. Coates JD, Bhupathiraju VK, Achenbach LA, Mclnerney MJ, Lovley DR. Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 2001; 51:581–588 [CrossRef][PubMed]
    [Google Scholar]
  13. Straub KL, Buchholz-Cleven BE. Geobacter bremensis sp. nov. and Geobacter pelophilus sp. nov., two dissimilatory ferric-iron-reducing bacteria. Int J Syst Evol Microbiol 2001; 51:1805–1808 [CrossRef][PubMed]
    [Google Scholar]
  14. Sung Y, Fletcher KE, Ritalahti KM, Apkarian RP, Ramos-Hernández N et al. Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 2006; 72:2775–2782 [CrossRef][PubMed]
    [Google Scholar]
  15. Nevin KP, Holmes DE, Woodard TL, Covalla SF, Lovley DR. Reclassification of Trichlorobacter thiogenes as Geobacter thiogenes comb. nov. Int J Syst Evol Microbiol 2007; 57:463–466 [CrossRef][PubMed]
    [Google Scholar]
  16. Shelobolina ES, Nevin KP, Blakeney-Hayward JD, Johnsen CV, Plaia TW et al. Geobacter pickeringii sp. nov., Geobacter argillaceus sp. nov. and Pelosinus fermentans gen. nov., sp. nov., isolated from subsurface kaolin lenses. Int J Syst Evol Microbiol 2007; 57:126–135 [CrossRef][PubMed]
    [Google Scholar]
  17. Shelobolina ES, Vrionis HA, Findlay RH, Lovley DR. Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation. Int J Syst Evol Microbiol 2008; 58:1075–1078 [CrossRef][PubMed]
    [Google Scholar]
  18. Kunapuli U, Jahn MK, Lueders T, Geyer R, Heipieper HJ et al. Desulfitobacterium aromaticivorans sp. nov. and Geobacter toluenoxydans sp. nov., iron-reducing bacteria capable of anaerobic degradation of monoaromatic hydrocarbons. Int J Syst Evol Microbiol 2010; 60:686–695 [CrossRef][PubMed]
    [Google Scholar]
  19. Prakash O, Gihring TM, Dalton DD, Chin K-J, Green SJ et al. Geobacter daltonii sp. nov., an Fe(III)- and uranium(VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination. Int J Syst Evol Microbiol 2010; 60:546–553 [CrossRef][PubMed]
    [Google Scholar]
  20. Viulu S, Nakamura K, Okada Y, Saitou S, Takamizawa K. Geobacter luticola sp. nov., an Fe(III)-reducing bacterium isolated from lotus field mud. Int J Syst Evol Microbiol 2013; 63:442–448 [CrossRef][PubMed]
    [Google Scholar]
  21. Sun D, Wang A, Cheng S, Yates M, Logan BE. Geobacter anodireducens sp. nov., an exoelectrogenic microbe in bioelectrochemical systems. Int J Syst Evol Microbiol 2014; 64:3485–3491 [CrossRef][PubMed]
    [Google Scholar]
  22. Zhou S, Yang G, Lu Q, Wu M. Geobacter soli sp. nov., a dissimilatory Fe(III)-reducing bacterium isolated from forest soil. Int J Syst Evol Microbiol 2014; 64:3786–3791 [CrossRef][PubMed]
    [Google Scholar]
  23. Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM et al. Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv Microb Physiol 2011; 59:1–99 [CrossRef][PubMed]
    [Google Scholar]
  24. Slobodkina GB, Kolganova TV, Querellou J, Bonch-Osmolovskaya EA, Slobodkin AI. Geoglobus acetivorans sp. nov., an iron(III)-reducing archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 2009; 59:2880–2883 [CrossRef][PubMed]
    [Google Scholar]
  25. Sleat R, Mah RA, Robinson R. Isolation and characterization of an anaerobic, cellulolytic bacterium, Clostridium cellulovorans sp. nov. Appl Environ Microbiol 1984; 48:88–93 [CrossRef][PubMed]
    [Google Scholar]
  26. Tschech A, Schink B. Fermentative degradation of resorcinol and resorcylic acids. Arch Microbiol 1985; 143:52–59 [CrossRef]
    [Google Scholar]
  27. Wolin EA, Wolin MJ, Wolfe RS. Formation of methane by bacterial extracts. J Biol Chem 1963; 238:2882–2886 [CrossRef][PubMed]
    [Google Scholar]
  28. Pérez-Rodríguez I, Rawls M, Coykendall DK, Foustoukos DI. Deferrisoma palaeochoriense sp. nov., a thermophilic, iron(III)-reducing bacterium from a shallow-water hydrothermal vent in the Mediterranean Sea. Int J Syst Evol Microbiol 2016; 66:830–836 [CrossRef][PubMed]
    [Google Scholar]
  29. Tully B, Savalia P, Abuyen K, Baughan C, Romero E et al. Genome sequence of Geothermobacter sp. strain EPR-M, a deep-sea hydrothermal vent iron reducer. Genome Announc 2017; 5:e00424–17 [CrossRef][PubMed]
    [Google Scholar]
  30. Emerson D. Potential for Iron-reduction and Iron-cycling in iron Oxyhydroxide-rich microbial mats at Loihi Seamount. Geomicrobiol J 2009; 26:639–647 [CrossRef]
    [Google Scholar]
  31. McBeth JM, Little BJ, Ray RI, Farrar KM, Emerson D. Neutrophilic iron-oxidizing "zetaproteobacteria" and mild steel corrosion in nearshore marine environments. Appl Environ Microbiol 2011; 77:1405–1412 [CrossRef][PubMed]
    [Google Scholar]
  32. Stookey LL. Ferrozine---a new spectrophotometric reagent for iron. Anal Chem 1970; 42:779–781 [CrossRef]
    [Google Scholar]
  33. Smith H, Abuyen K, Tremblay J, Savalia P, Pérez-Rodríguez I et al. Genome sequence of Geothermobacter sp. strain HR-1, an Iron reducer from the Lō'ihi Seamount, Hawai'i. Genome Announc 2018; 6:e00339–18 [CrossRef][PubMed]
    [Google Scholar]
  34. Orcutt B, Wheat CG, Edwards KJ. Subseafloor Ocean crust microbial Observatories: development of FLOCS (flow-through Osmo colonization system) and evaluation of Borehole construction materials. Geomicrobiol J 2010; 27:143–157 [CrossRef]
    [Google Scholar]
  35. Forget NL, Murdock SA, Juniper SK. Bacterial diversity in Fe-rich hydrothermal sediments at two South Tonga Arc submarine volcanoes. Geobiology 2010; 8:417–432 [CrossRef][PubMed]
    [Google Scholar]
  36. Darjany LE, Whitcraft CR, Dillon JG. Lignocellulose-responsive bacteria in a southern California salt marsh identified by stable isotope probing. Front Microbiol 2014; 5:263 [CrossRef][PubMed]
    [Google Scholar]
  37. Na S-I, Kim YO, Yoon S-H, Ha S-M, Baek I et al. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 2018; 56:280–285 [CrossRef][PubMed]
    [Google Scholar]
  38. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 2017; 110:1281–1286 [CrossRef][PubMed]
    [Google Scholar]
  39. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [CrossRef][PubMed]
    [Google Scholar]
  40. 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 [CrossRef][PubMed]
    [Google Scholar]
  41. Miller LT. A single derivatization method for bacterial fatty acid methyl esters including hydroxy acids. J Clin Microbiol 1982; 16:584–586
    [Google Scholar]
  42. Kuykendall LD, Roy MA, O'Neill JJ, Devine TE. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum . Int J Syst Bacteriol 1988; 38:358–361 [CrossRef]
    [Google Scholar]
  43. Euzéby JP. Validation List no. 102. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 2005; 55:547–549
    [Google Scholar]
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