1887

Abstract

A novel member of the phylum Verrucomicrobia was isolated from an oilsands tailings pond in Alberta, Canada. Cells of isolate NVT are Gram-negative, strictly aerobic, non-pigmented, non-motile cocci to diplococci 0.5–1.0 µm in diameter. The bacterium is neutrophilic (optimum pH 6.0–8.0) but alkalitolerant, capable of growth between pH 5.5 and 11.0. The temperature range for growth is 15–40 °C (optimum 25–37 °C). Carbon and energy sources include sugars and organic acids. Nitrogen sources include nitrate, urea, l-glycine, l-alanine, l-proline and l-serine. Does not fix atmospheric nitrogen. Does not require NaCl and is inhibited at NaCl concentrations above 3.0 % (w/v). The DNA G+C content of strain NVT, based on a draft genome sequence, is 66.1 mol%. MK-6 and MK-7 are the major respiratory quinones. Major cellular fatty acids are anteiso-C15 : 0 and iso-C15 : 0. Phylogenetic analysis of 16S rRNA gene sequences revealed that the strain belongs to the family Opitutaceae of the phylum Verrucomicrobia . The most closely related validated species is Opitutus terrae (93.7 % 16S rRNA gene sequence identity to its type strain PB90-1). Based on genotypic, phenotypic and chemotaxonomic characteristics, it was concluded that this strain represents a novel genus and species, for which the name Oleiharenicola alkalitolerans gen. nov., sp. nov. is proposed. The type strain of this novel species is NVT (=ATCC BAA-2697;=DSM 29249).

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2018-02-20
2019-10-24
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References

  1. Hedlund BP, Gosink JJ, Staley JT. Verrucomicrobia div. nov., a new division of the bacteria containing three new species of Prosthecobacter. Antonie van Leeuwenhoek 1997;72:29–38 [CrossRef][PubMed]
    [Google Scholar]
  2. Freitas S, Hatosy S, Fuhrman JA, Huse SM, Welch DB et al. Global distribution and diversity of marine Verrucomicrobia. ISME J 2012;6:1499–1505 [CrossRef][PubMed]
    [Google Scholar]
  3. Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB et al. Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 2007;450:879–882 [CrossRef][PubMed]
    [Google Scholar]
  4. Sharp CE, Smirnova AV, Graham JM, Stott MB, Khadka R et al. Distribution and diversity of Verrucomicrobia methanotrophs in geothermal and acidic environments. Environ Microbiol 2014;16:1867–1878 [CrossRef][PubMed]
    [Google Scholar]
  5. Lau MC, Aitchison JC, Pointing SB. Bacterial community composition in thermophilic microbial mats from five hot springs in central Tibet. Extremophiles 2009;13:139–149 [CrossRef][PubMed]
    [Google Scholar]
  6. Chin KJ, Liesack W, Janssen PH. Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division 'Verrucomicrobia' isolated from rice paddy soil. Int J Syst Evol Microbiol 2001;51:1965–1968 [CrossRef][PubMed]
    [Google Scholar]
  7. Lindström ES, Kamst-van Agterveld MP, Zwart G. Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl Environ Microbiol 2005;71:8201–8206 [CrossRef][PubMed]
    [Google Scholar]
  8. Lindström ES. Response of a member of the Verrucomicrobia, among the dominating bacteria in a hypolimnion, to increased phosphorus availability. J Plankton Res 2004;26:241–246 [CrossRef]
    [Google Scholar]
  9. Hongoh Y, Ohkuma M, Kudo T. Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 2003;44:231–242 [CrossRef][PubMed]
    [Google Scholar]
  10. Hedlund BP. Phylum XXIII. Verrucomicrobia phyl. nov. In Krieg NR. (editor) Bergey’s Manual® of Syst Bacteriol New York, NY: Springer; 2010; pp.795–841
    [Google Scholar]
  11. Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998;180:4765–4774[PubMed]
    [Google Scholar]
  12. Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG et al. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 2011;43:1450–1455 [CrossRef][PubMed]
    [Google Scholar]
  13. Bowman JS, Rasmussen S, Blom N, Deming JW, Rysgaard S et al. Microbial community structure of Arctic multiyear sea ice and surface seawater by 454 sequencing of the 16S RNA gene. ISME J 2012;6:11–20 [CrossRef][PubMed]
    [Google Scholar]
  14. Fan LM, Barry K, Hu GD, Meng S, Song C et al. Bacterioplankton community analysis in tilapia ponds by Illumina high-throughput sequencing. World J Microbiol Biotechnol 2016;32:1–11 [CrossRef][PubMed]
    [Google Scholar]
  15. Wu DX, Zhao SM, Peng N, Cp X, Wang J et al. Effects of a probiotic (Bacillus subtilis FY99‐01) on the bacterial community structure and composition of shrimp (Litopenaeus vannamei, Boone) culture water assessed by denaturing gradient gel electrophoresis and high‐throughput sequencing. Aquaculture Res 2014;31:857–869
    [Google Scholar]
  16. Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JLM. Correction for Wertz et al., "Genomic and physiological characterization of the Verrucomicrobia isolate Didymococcus colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes". Appl Environ Microbiol 2017;83:e00987-17 [CrossRef][PubMed]
    [Google Scholar]
  17. Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JL. Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl Environ Microbiol 2012;78:1544–1555 [CrossRef][PubMed]
    [Google Scholar]
  18. Rast P, Glöckner I, Boedeker C, Jeske O, Wiegand S et al. Three novel species with peptidoglycan cell walls form the new genus Lacunisphaera gen. nov. in the family Opitutaceae of the verrucomicrobial subdivision 4. Front Microbiol 2017;8:202 [CrossRef][PubMed]
    [Google Scholar]
  19. Shieh WY, Jean WD. Alterococcus agarolyticus, gen.nov., sp.nov., a halophilic thermophilic bacterium capable of agar degradation. Can J Microbiol 1998;44:637–645 [CrossRef][PubMed]
    [Google Scholar]
  20. Lin JY, Russell JA, Sanders JG, Wertz JT. Cephaloticoccus gen. nov., a new genus of 'Verrucomicrobia' containing two novel species isolated from Cephalotes ant guts. Int J Syst Evol Microbiol 2016;66:3034–3040 [CrossRef][PubMed]
    [Google Scholar]
  21. van Passel MW, Kant R, Palva A, Copeland A, Lucas S et al. Genome sequence of the verrucomicrobium Opitutus terrae PB90-1, an abundant inhabitant of rice paddy soil ecosystems. J Bacteriol 2011;193:2367–2368 [CrossRef][PubMed]
    [Google Scholar]
  22. Quagraine EK, Peterson HG, Headley JV. In situ bioremediation of naphthenic acids contaminated tailing pond waters in the Athabasca oil sands region–demonstrated field studies and plausible options: a review. J Environ Sci Health A Tox Hazard Subst Environ Eng 2005;40:685–722 [CrossRef][PubMed]
    [Google Scholar]
  23. Saidi-Mehrabad A, He Z, Tamas I, Sharp CE, Brady AL et al. Methanotrophic bacteria in oilsands tailings ponds of northern Alberta. ISME J 2012;7:908–921 [CrossRef][PubMed]
    [Google Scholar]
  24. Heyer J, Galchenko VF, Dunfield PF. Molecular phylogeny of type II methane-oxidizing bacteria isolated from various environments. Microbiology 2002;148:2831–2846 [CrossRef][PubMed]
    [Google Scholar]
  25. Doronina NV, Darmaeva TD, Trotsenko YA. Novel aerobic methylotrophic isolates from the soda lakes of the southern Transbaikal region. Microbiology 2001;70:342–348 [CrossRef]
    [Google Scholar]
  26. Fulthorpe RR, Liss SN, Allen DG. Characterization of bacteria isolated from a bleached kraft pulp mill wastewater treatment system. Can J Microbiol 1993;39:13–24 [CrossRef][PubMed]
    [Google Scholar]
  27. Raj HD. Oligotrophic methylotrophs: Ancylobacter (basonym "Microcyclus" Orskov) Raj gen. nov. Crit Rev Microbiol 1989;17:89–106 [CrossRef][PubMed]
    [Google Scholar]
  28. Xin YH, Zhou YG, Chen WX. Ancylobacter polymorphus sp. nov. and Ancylobacter vacuolatus sp. nov. Int J Syst Evol Microbiol 2006;56:1185–1188 [CrossRef][PubMed]
    [Google Scholar]
  29. Zaichikova MV, Berestovskaya YY, Akimov VN, Kizilova AK, Vasilieva LV. Ancylobacter abiegnus sp. nov., an oligotrophic member of the xylotrophic mycobacterial community. Microbiology 2010;79:483–490 [CrossRef]
    [Google Scholar]
  30. Reasoner DJ, Geldreich EE. A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 1985;49:1–7[PubMed]
    [Google Scholar]
  31. Kim JJ, Kim HN, Masui R, Kuramitsu S, Seo JH et al. Isolation of uncultivable anaerobic thermophiles of the family Clostridiaceae requiring growth-supporting factors. J Microbiol Biotechnol 2008;18:611–615[PubMed]
    [Google Scholar]
  32. Moyes RB, Reynolds J, Breakwell DP. Differential staining of bacteria: Gram stain. Curr Protoc Microbiol 2009;15:A.3C.1–A.3C.8 [CrossRef][PubMed]
    [Google Scholar]
  33. Shields P, Cathcart L. Motility test medium protocol. In Laboratory Protocols Washington, DC: Springer-American Society for Microbiology; pp.3–4
    [Google Scholar]
  34. Sinninghe Damsté JS, Rijpstra WIC, Hopmans EC, Weijers JWH, Foesel BU et al. 13,16-Dimethyl octacosanedioic acid (iso-diabolic acid), a common membrane-spanning lipid of Acidobacteria subdivisions 1 and 3. Appl Environ Microbiol 2011;77:4147–4154 [CrossRef][PubMed]
    [Google Scholar]
  35. Collins MD, Pirouz T, Goodfellow M, Minnikin DE. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol 1977;100:221–230 [CrossRef][PubMed]
    [Google Scholar]
  36. Groth I, Schumann P, Rainey FA, Martin K, Schuetze B et al. Demetria terragena gen. nov., sp. nov., a new genus of actinomycetes isolated from compost soil. Int J Syst Bacteriol 1997;47:1129–1133 [CrossRef][PubMed]
    [Google Scholar]
  37. Lee J, Park B, Woo SG, Lee J, Park J et al. Prosthecobacter algae sp. nov., isolated from activated sludge using algal metabolites. Int J Syst Evol Microbiol 2014;64:663–667 [CrossRef][PubMed]
    [Google Scholar]
  38. Yoon J, Yasumoto-Hirose M, Katsuta A, Sekiguchi H, Matsuda S et al. Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum 'Verrucomicrobia' isolated from seawater in Japan. Int J Syst Evol Microbiol 2007;57:959–963 [CrossRef][PubMed]
    [Google Scholar]
  39. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008;18:821–829 [CrossRef][PubMed]
    [Google Scholar]
  40. Markowitz VM, Korzeniewski F, Palaniappan K, Szeto E, Werner G et al. The integrated microbial genomes (IMG) system. Nucleic Acids Res 2006;34:D344–D348 [CrossRef][PubMed]
    [Google Scholar]
  41. Mavromatis K, Ivanova NN, Chen IM, Szeto E, Markowitz VM et al. The DOE-JGI standard operating procedure for the annotations of microbial genomes. Stand Genomic Sci 2009;1:63–67 [CrossRef][PubMed]
    [Google Scholar]
  42. Chen LH, Kenyon GL, Curtin F, Harayama S, Bembenek ME et al. 4-Oxalocrotonate tautomerase, an enzyme composed of 62 amino acid residues per monomer. J Biol Chem 1992;267:17716–17721[PubMed]
    [Google Scholar]
  43. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  44. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 2012;62:716–721 [CrossRef][PubMed]
    [Google Scholar]
  45. 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 [CrossRef][PubMed]
    [Google Scholar]
  46. Ludwig W, Strunk O, Westram R, Richter L, Meier H et al. ARB: a software environment for sequence data. Nucleic Acids Res 2004;32:1363–1371 [CrossRef][PubMed]
    [Google Scholar]
  47. Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012;28:1823–1829 [CrossRef][PubMed]
    [Google Scholar]
  48. Meier-Kolthoff JP, Klenk HP, 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 [CrossRef][PubMed]
    [Google Scholar]
  49. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010;27:221–224 [CrossRef][PubMed]
    [Google Scholar]
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