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Abstract

Three novel carbon monoxide-oxidizing Halobacteria were isolated from Bonneville Salt Flats (Utah, USA) salt crusts and nearby saline soils. Phylogenetic analysis of 16S rRNA gene sequences revealed that strains PCN9, WSA2 and WSH3 belong to the genera , and , respectively. Strains PCN9, WSA2 and WSH3 grew optimally at 40 °C (PCN9) or 50 °C (WSA2, WSH3). NaCl optima were 3 M (PCN9, WSA2) or 4 M NaCl (WSH3). Carbon monoxide was oxidized by all isolates, each of which contained a molybdenum-dependent CO dehydrogenase. G+C contents for the three respective isolates were 66.75, 67.62, and 63.97 mol% as derived from genome analyses. The closest phylogenetic relatives for PCN9, WSA2 and WSH3 were A1, D90 and EB27 with 98.71, 98.19 and 95.95 % 16S rRNA gene sequence similarities, respectively. Genome comparisons of PCN9 with A1 yielded an average nucleotide identity (ANI) of 82.0% and a digital DNA–DNA hybridization (dDDH) value of 25.7 %; comparisons of WSA2 with D90 yielded ANI and dDDH values of 86.34 and 31.1 %, respectively. The ANI value for a comparison of WSH3 with EB27 was 75.2 %. Physiological, biochemical, genetic and genomic characteristics of PCN9, WSA2 and WSH3 differentiated them from their closest phylogenetic neighbours and indicated that they represent novel species for which the names , and are proposed, respectively. The type strains are PCN9 (=JCM 32472=LMG 31022=ATCC TSD-126), WSA2 (=JCM 32473=ATCC TSD-127) and WSH3 (=JCM 32474=ATCC TSD-128).

Funding
This study was supported by the:
  • Gary King , National Aeronautics and Space Administration , (Award 15-EXO15_2-0147)
  • Gary King , National Science Foundation , (Award EAR-1565499)
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2020-06-22
2020-11-25
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References

  1. Oren A. Halophilic microbial communities and their environments. Curr Opin Biotechnol 2015; 33:119–124 [CrossRef][PubMed]
    [Google Scholar]
  2. Ventosa A, de la Haba RR, Sánchez-Porro C, Papke RT. Microbial diversity of hypersaline environments: a metagenomic approach. Curr Opin Microbiol 2015; 25:80–87 [CrossRef][PubMed]
    [Google Scholar]
  3. Mora-Ruiz MDR, Cifuentes A, Font-Verdera F, Pérez-Fernández C, Farias ME et al. Biogeographical patterns of bacterial and archaeal communities from distant hypersaline environments. Syst Appl Microbiol 2018; 41:139–150 [CrossRef][PubMed]
    [Google Scholar]
  4. King GM, Weber CF. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 2007; 5:107118 [CrossRef][PubMed]
    [Google Scholar]
  5. Khalil M, Pinto J, Shearer M. Atmospheric carbon monoxide. Chemosphere-Global change science; 1999; 1
  6. King GM. Characteristics and significance of atmospheric carbon monoxide consumption by soils. Chemosphere - Global Change Science 1999; 1:53–63 [CrossRef]
    [Google Scholar]
  7. McDuff S, King GM, Neupane S, Myers MR. Isolation and characterization of extremely halophilic CO-oxidizing euryarchaeota from hypersaline cinders, sediments and soils and description of a novel CO oxidizer, Haloferax namakaokahaiae Mke2.3T, sp. nov. FEMS Microbiol Ecol 2016; 92:fiw028 [CrossRef][PubMed]
    [Google Scholar]
  8. Myers MR, King GM. Perchlorate-coupled carbon monoxide (CO) oxidation: evidence for a plausible microbe-mediated reaction in Martian brines. Front Microbiol 2017; 8:2571 [CrossRef][PubMed]
    [Google Scholar]
  9. Myers MR, King GM. Addendum: Perchlorate-Coupled carbon monoxide (CO) oxidation: evidence for a plausible Microbe-Mediated reaction in Martian brines. Front Microbiol 2019; 10: [CrossRef]
    [Google Scholar]
  10. Lines GC. Hydrology and surface morphology of the Bonneville salt flats and pilot Valley playa, Utah: dept. of the interior. Geological Survey 1979
    [Google Scholar]
  11. Jewell P, Nelson D, Bowen B, Raming L. Insights into Lake Bonneville Using Remote Sensing and Digital Terrain Tools Developments in Earth Surface Processes: Elsevier; 2016 pp 598–616
    [Google Scholar]
  12. Bowen BB, Kipnis EL, Raming LW. Temporal dynamics of flooding, evaporation, and desiccation cycles and observations of salt crust area change at the Bonneville salt flats, Utah. Geomorphology 2017; 299:1–11 [CrossRef]
    [Google Scholar]
  13. Oren A, Ventosa A, Grant W. Proposed minimal standards for description of new taxa in the order Halobacteriales. International journal of systematic and evolutionary microbiology 1997; 47:233–238
    [Google Scholar]
  14. Oren A. Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Systems 2008; 4:2 [CrossRef][PubMed]
    [Google Scholar]
  15. Dyall-Smith M. The Halohandbook: Protocols for Haloarchaeal Genetics 14 Melbourne: Haloarchaeal Genetics Laboratory; 2008
    [Google Scholar]
  16. Miyashita A, Mochimaru H, Kazama H, Ohashi A, Yamaguchi T et al. Development of 16S rRNA gene-targeted primers for detection of archaeal anaerobic methanotrophs (ANMEs). FEMS Microbiol Lett 2009; 297:31–37 [CrossRef][PubMed]
    [Google Scholar]
  17. DeLong EF. Archaea in coastal marine environments. Proc Natl Acad Sci U S A 1992; 89:5685–5689 [CrossRef][PubMed]
    [Google Scholar]
  18. Lane D. 16S/23S rRNA sequencing. nucleic acid techniques in bacterial Systematics; 1991115–175
  19. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically United database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:16131617 [CrossRef][PubMed]
    [Google Scholar]
  20. Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G et al. Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum . Extremophiles 2004; 8:431–439 [CrossRef][PubMed]
    [Google Scholar]
  21. Chen S, Xu Y, Liu H-C, Yang A-N, Ke L-X. Halobaculum roseum sp. nov., isolated from underground salt deposits. Int J Syst Evol Microbiol 2017; 67:818–823 [CrossRef][PubMed]
    [Google Scholar]
  22. Makhdoumi-Kakhki A, Amoozegar MA, Ventosa A. Halovenus aranensis gen. nov., sp. nov., an extremely halophilic archaeon from Aran-Bidgol salt lake. Int J Syst Evol Microbiol 2012; 62:1331–1336 [CrossRef][PubMed]
    [Google Scholar]
  23. 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; 12:635645 [CrossRef][PubMed]
    [Google Scholar]
  24. Nei M, Kumar S. Molecular Evolution and Phylogenetics Oxford university press; 2000
    [Google Scholar]
  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed]
    [Google Scholar]
  26. Stecher G, Tamura K, Kumar S. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol 2020; 37:1237–1239 [CrossRef][PubMed]
    [Google Scholar]
  27. Coil D, Jospin G, Darling AE. A5-miseq: an updated pipeline to assemble microbial genomes from illumina MiSeq data. Bioinformatics 2015; 31:587–589 [CrossRef][PubMed]
    [Google Scholar]
  28. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [CrossRef][PubMed]
    [Google Scholar]
  29. Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res 2014; 42:D560–D567 [CrossRef][PubMed]
    [Google Scholar]
  30. Mukherjee S, Stamatis D, Bertsch J, Ovchinnikova G, Katta HY et al. Genomes online database (gold) v.7: updates and new features. Nucleic Acids Res 2019; 47:D649–D659 [CrossRef]
    [Google Scholar]
  31. 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]
  32. 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]
  33. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911–917 [CrossRef][PubMed]
    [Google Scholar]
  34. Tindall BJ. A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 1990; 13:128–130 [CrossRef]
    [Google Scholar]
  35. Tindall BJ, Sikorski J, Smibert RA, Krieg NR. Phenotypic characterization and the principles of comparative systematics. Methods for General and Molecular Microbiology, 3rd ed. American Society of Microbiology; 2007 pp 330–393
    [Google Scholar]
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