1887

Abstract

Two extremely halophilic archaea, strains Cb34 and C170, belonging to the genus , were isolated from the brine of the hypersaline lake Aran-Bidgol in Iran. Cells of the two strains were motile, pleomorphic rods, stained Gram-variable and produced red-pigmented colonies. Strains Cb34 and C170 required 25 % (w/v) salts, pH 7.0 and 37 °C for optimal growth under aerobic conditions; 0.3 M Mg was required. Cells of both isolates were lysed in distilled water and hypotonic treatment with < 10 % NaCl provoked cell lysis. Phylogenetic analysis based on 16S rRNA gene sequence similarities showed that these two strains were closely related to B31 (98.8 %) and other members of the genus . In addition, studies based on the ′ gene revealed that strains Cb34 and C170 are placed among the species of and are closely related to B31, with ′ gene sequence similarity less than or equal to 95.7 %. The polar lipid patterns of both strains consisted of phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester, phosphatidylglycerol sulfate and sulfated mannosyl glucosyl diether. The DNA G+C content was 62.1–62.4 mol%. DNA–DNA hybridization studies confirmed that strains Cb34 and C170 constitute a distinct species. Data obtained in this study show that the two strains represent a novel species, for which the name sp. nov. is proposed. The type strain is Cb34 ( = CECT 8745 = IBRC-M 10233).

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2016-01-01
2020-01-27
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References

  1. Akaike H.. 1974; A new look at the statistical model identification. IEEE Trans Automat Contr19:716–723 [CrossRef]
    [Google Scholar]
  2. Allers T., Ngo H. P., Mevarech M., Lloyd R. G.. 2004; Development of additional selectable markers for the halophilic archaeon Haloferax volcanii based on the leuB and trpA genes. Appl Environ Microbiol70:943–953 [CrossRef][PubMed]
    [Google Scholar]
  3. Amoozegar M. A., Makhdoumi-Kakhki A., Shahzadeh Fazeli S. A., Azarbaijani R., Ventosa A.. 2012; Halopenitus persicus gen. nov., sp. nov., an archaeon from an inland salt lake. Int J Syst Evol Microbiol62:1932–1936 [CrossRef][PubMed]
    [Google Scholar]
  4. Amoozegar M. A., Makhdoumi-Kakhki A., Mehrshad M., Fazeli S. A., Ventosa A.. 2013; Halopenitus malekzadehii sp. nov., an extremely halophilic archaeon isolated from a salt lake. Int J Syst Evol Microbiol63:3232–3236 [CrossRef][PubMed]
    [Google Scholar]
  5. Amoozegar M. A., Makhdoumi-Kakhki A., Mehrshad M., Fazeli S. A., Spröer C., Ventosa A.. 2014a; Halorientalis persicus sp. nov., an extremely halophilic archaeon isolated from a salt lake and emended description of the genus Halorientalis . Int J Syst Evol Microbiol64:940–944 [CrossRef][PubMed]
    [Google Scholar]
  6. Amoozegar M. A., Makhdoumi-Kakhki A., Mehrshad M., Riazi S., Ventosa A.. 2014b; Halovivax limisalsi sp. nov., an extremely halophilic archaeon from hypersaline mud. Int J Syst Evol Microbiol64:3422–3426 [CrossRef][PubMed]
    [Google Scholar]
  7. Amoozegar M. A., Makhdoumi-Kakhki A., Mehrshad M., Rasooli M., Fazeli S. A., Spröer C., Ventosa A.. 2015; Halovivax cerinus sp. nov., an extremely halophilic archaeon from a hypersaline lake. Int J Syst Evol Microbiol65:65–70 [CrossRef][PubMed]
    [Google Scholar]
  8. Angelini R., Corral P., Lopalco P., Ventosa A., Corcelli A.. 2012; Novel ether lipid cardiolipins in archaeal membranes of extreme haloalkaliphiles. Biochim Biophys Acta1818:1365–1373 [CrossRef][PubMed]
    [Google Scholar]
  9. Arahal D. R., Dewhirst F. E., Paster B. J., Volcani B. E., Ventosa A.. 1996; Phylogenetic analyses of some extremely halophilic archaea isolated from Dead Sea water, determined on the basis of their 16S rRNA sequences. Appl Environ Microbiol62:3779–3786[PubMed]
    [Google Scholar]
  10. Barrow G. I., Feltham R. K. A.. 2003; Cowan and Steel's Manual for the Identification of Medical Bacteria, 3rd edn. Cambridge: Cambridge University Press;
    [Google Scholar]
  11. Bauer A. W., Kirby W. M. M., Sherris J. C., Turck M.. 1966; Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol45:493–496[PubMed]
    [Google Scholar]
  12. Boucher Y., Douady C. J., Sharma A. K., Kamekura M., Doolittle W. F.. 2004; Intragenomic heterogeneity and intergenomic recombination among haloarchaeal rRNA genes. J Bacteriol186:3980–3990 [CrossRef][PubMed]
    [Google Scholar]
  13. Corcelli A., Lobasso S.. 2006; Characterization of lipids of halophilic archaea. Methods Microbiol35:585–613 [CrossRef]
    [Google Scholar]
  14. Corral P., Gutiérrez M. C., Castillo A. M., Domínguez M., Lopalco P., Corcelli A., Ventosa A.. 2013; Natronococcus roseus sp. nov., a haloalkaliphilic archaeon from a hypersaline lake. Int J Syst Evol Microbiol63:104–108 [CrossRef][PubMed]
    [Google Scholar]
  15. Cui H. L., Tohty D., Zhou P. J., Liu S. J.. 2006; Halorubrum lipolyticum sp. nov. and Halorubrum aidingense sp. nov., isolated from two salt lakes in Xin-Jiang, China. Int J Syst Evol Microbiol56:1631–1634 [CrossRef][PubMed]
    [Google Scholar]
  16. Darriba D., Taboada G. L., Doallo R., Posada D.. 2012; jModelTest 2: more models, new heuristics and parallel computing. Nat Methods9:772 [CrossRef][PubMed]
    [Google Scholar]
  17. DeLong E. F.. 1992; Archaea in coastal marine environments. Proc Natl Acad Sci U S A89:5685–5689 [CrossRef][PubMed]
    [Google Scholar]
  18. Dussault H. P.. 1955; An improved technique for staining red halophilic bacteria. J Bacteriol70:484–485[PubMed]
    [Google Scholar]
  19. Dyall-Smith M.. 2009; The Halohandbook: Protocols for Haloarchaeal Genetics version 7.2 http://www.haloarchaea.com/resources/halohandbook/
    [Google Scholar]
  20. Edgar R. C.. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  21. Enache M., Itoh T., Fukushima T., Usami R., Dumitru L., Kamekura M.. 2007; Phylogenetic relationships within the family Halobacteriaceae inferred from rpoB′ gene and protein sequences. Int J Syst Evol Microbiol57:2289–2295 [CrossRef][PubMed]
    [Google Scholar]
  22. Fan H., Xue Y., Ma Y., Ventosa A., Grant W. D.. 2004; Halorubrum tibetense sp. nov., a novel haloalkaliphilic archaeon from Lake Zabuye in Tibet, China. Int J Syst Evol Microbiol54:1213–1216 [CrossRef][PubMed]
    [Google Scholar]
  23. Felsenstein J.. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution39:783–791 [CrossRef]
    [Google Scholar]
  24. Feng J., Zhou P., Zhou Y. G., Liu S. J., Warren-Rhodes K.. 2005; Halorubrum alkaliphilum sp. nov., a novel haloalkaliphile isolated from a soda lake in Xinjiang, China. Int J Syst Evol Microbiol55:149–152 [CrossRef][PubMed]
    [Google Scholar]
  25. Fernández A. B., Ghai R., Martin-Cuadrado A. B., Sánchez-Porro C., Rodriguez-Valera F., Ventosa A.. 2014a; Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiol Ecol88:623–635 [CrossRef][PubMed]
    [Google Scholar]
  26. Fernández A. B., Vera-Gargallo B., Sánchez-Porro C., Ghai R., Papke R. T., Rodriguez-Valera F., Ventosa A.. 2014b; Comparison of prokaryotic community structure from Mediterranean and Atlantic saltern concentrator ponds by a metagenomic approach. Front Microbiol5:196[PubMed][CrossRef]
    [Google Scholar]
  27. Fuchs B., Schiller J., Süß R., Schürenberg M., Suckau D.. 2007; A direct and simple method of coupling matrix-assisted laser desorption and ionization time-of-flight mass spectrometry (MALDI-TOF MS) to thin-layer chromatography (TLC) for the analysis of phospholipids from egg yolk. Anal Bioanal Chem389:827–834 [CrossRef][PubMed]
    [Google Scholar]
  28. Fullmer M. S., Soucy S. M., Swithers K. S., Makkay A. M., Wheeler R., Ventosa A., Gogarten J. P., Papke R. T.. 2014; Population and genomic analysis of the genus Halorubrum . Front Microbiol5:140[PubMed][CrossRef]
    [Google Scholar]
  29. Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R.. editors 1994; Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology;
    [Google Scholar]
  30. Ghai R., Pašić L., Fernández A. B., Martin-Cuadrado A. B., Mizuno C. M., McMahon K. D., Papke R. T., Stepanauskas R., Rodriguez-Brito B., other authors. 2011; New abundant microbial groups in aquatic hypersaline environments. Sci Rep1:135 [CrossRef][PubMed]
    [Google Scholar]
  31. Gouy M., Guindon S., Gascuel O.. 2010; SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol27:221–224 [CrossRef][PubMed]
    [Google Scholar]
  32. Grant W. D., Kamekura M., McGenity T. J., Ventosa A.. 2001; Class III. Halobacteria class. nov. In Bergey's Manual of Systematic Bacteriology, 2nd edn.vol. 1 pp294–301Edited by Boone D. R., Castenholz R. W., Garrity G. M.. New York: Springer;
    [Google Scholar]
  33. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O.. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  34. Gutiérrez M. C., Castillo A. M., Pagaling E., Heaphy S., Kamekura M., Xue Y., Ma Y., Cowan D. A., Jones B. E., other authors. 2008; Halorubrum kocurii sp. nov., an archaeon isolated from a saline lake. Int J Syst Evol Microbiol58:2031–2035 [CrossRef][PubMed]
    [Google Scholar]
  35. Gutiérrez M. C., Castillo A. M., Corral P., Kamekura M., Ventosa A.. 2011; Halorubrum aquaticum sp. nov., an archaeon isolated from hypersaline lakes. Int J Syst Evol Microbiol61:1144–1148 [CrossRef][PubMed]
    [Google Scholar]
  36. Johnson J. L.. 1994; Similarity analysis of DNAs. In Methods for General and Molecular Bacteriology pp655–682Edited by Gerhardt P., Murray R. G. E., Wood W. A., Krieg N. R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  37. Kates M.. 1986; Laboratory techniques. In Techniques of Lipidology pp100–110Edited by Burdon R. H., van Knippenberg P. H.. Amsterdam: Elsevier;
    [Google Scholar]
  38. Kean E. L.. 1968; Rapid, sensitive spectrophotometric method for quantitative determination of sulfatides. J Lipid Res9:319–327[PubMed]
    [Google Scholar]
  39. Kim O. S., Cho Y. J., Lee K., Yoon S. H., Kim M., Na H., Park S. C., Jeon Y. S., Lee J. H., other authors. 2012; Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol62:716–721 [CrossRef][PubMed]
    [Google Scholar]
  40. Ludwig W., Strunk O., Westram R., Richter L., Meier H., Yadhukumar, Buchner A., Lai T., Steppi S., other authors. 2004; arb: a software environment for sequence data. Nucleic Acids Res32:1363–1371 [CrossRef][PubMed]
    [Google Scholar]
  41. Maddison W. P., Maddison D. R.. 2011; Mesquite: a Modular System for Evolutionary Analysis, version 2.75http://mesquiteproject.org
    [Google Scholar]
  42. Makhdoumi-Kakhki A., Amoozegar M. A., Kazemi B., Pašić L., Ventosa A.. 2012a; Prokaryotic diversity in Aran-Bidgol salt lake, the largest hypersaline playa in Iran. Microbes Environ27:87–93 [CrossRef][PubMed]
    [Google Scholar]
  43. Makhdoumi-Kakhki A., Amoozegar M. A., Bagheri M., Ramezani M., Ventosa A.. 2012b; Haloarchaeobius iranensis gen. nov., sp. nov., an extremely halophilic archaeon isolated from a saline lake. Int J Syst Evol Microbiol62:1021–1026 [CrossRef][PubMed]
    [Google Scholar]
  44. Makhdoumi-Kakhki A., Amoozegar M. A., Ventosa A.. 2012c; Halovenus aranensis gen. nov., sp. nov., an extremely halophilic archaeon from Aran-Bidgol salt lake. Int J Syst Evol Microbiol62:1331–1336 [CrossRef][PubMed]
    [Google Scholar]
  45. Mancinelli R. L., Landheim R., Sánchez-Porro C., Dornmayr-Pfaffenhuemer M., Gruber C., Legat A., Ventosa A., Radax C., Ihara K., other authors. 2009; Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico, Western Australia and Naxos, Greece. Int J Syst Evol Microbiol59:1908–1913 [CrossRef][PubMed]
    [Google Scholar]
  46. Marmur J.. 1961; A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol3:208–218 [CrossRef]
    [Google Scholar]
  47. Marmur J., Doty P.. 1962; Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol5:109–118 [CrossRef][PubMed]
    [Google Scholar]
  48. McGenity T. J., Grant W. D.. 1995; Transfer of Halobacterium saccharovorum, Halobacterium sodomense, Halobacterium trapanicum NRC 34021 and Halobacterium lacusprofundi to the genus Halorubrum gen. nov., as Halorubrum saccharovorum comb. nov., Halorubrum sodomense comb. nov., Halorubrum trapanicum comb. nov., and Halorubrum lacusprofundi comb. nov. Syst Appl Microbiol18:237–243 [CrossRef]
    [Google Scholar]
  49. McGenity T. J., Grant W. D.. 2001; Genus VII. Halorubrum . In Bergey's Manual of Systematic Bacteriology, 2nd edn.vol. 1 pp320–324Edited by Boone D. R., Castenholz R. W., Garrity G. M.. New York: Springer;
    [Google Scholar]
  50. Minegishi H., Kamekura M., Itoh T., Echigo A., Usami R., Hashimoto T.. 2010; Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B′ (rpoB′) gene. Int J Syst Evol Microbiol60:2398–2408 [CrossRef][PubMed]
    [Google Scholar]
  51. Oren A.. 2012; Taxonomy of the family Halobacteriaceae: a paradigm for changing concepts in prokaryote systematics. Int J Syst Evol Microbiol62:263–271[CrossRef]
    [Google Scholar]
  52. Oren A., Ventosa A., Grant W. D.. 1997; Proposed minimal standards for description of new taxa in the order Halobacteriales . Int J Syst Bacteriol47:233–238 [CrossRef]
    [Google Scholar]
  53. Oren A., Arahal D. R., Ventosa A.. 2009; Emended descriptions of genera of the family Halobacteriaceae . Int J Syst Evol Microbiol59:637–642 [CrossRef][PubMed]
    [Google Scholar]
  54. Owen R. J., Pitcher D.. 1985; Current methods for estimating DNA base composition and levels of DNA–DNA hybridization. In Chemical Methods in Bacterial Systematics pp67–93Edited by Goodfellow M., Minnikin D. E.. London: Academic Press;
    [Google Scholar]
  55. Papke R. T., Koenig J. E., Rodríguez-Valera F., Doolittle W. F.. 2004; Frequent recombination in a saltern population of Halorubrum . Science306:1928–1929[PubMed]
    [Google Scholar]
  56. Papke R. T., Zhaxybayeva O., Feil E. J., Sommerfeld K., Muise D., Doolittle W. F.. 2007; Searching for species in haloarchaea. Proc Natl Acad Sci U S A104:14092–14097 [CrossRef][PubMed]
    [Google Scholar]
  57. Papke R. T., White E., Reddy P., Weigel G., Kamekura M., Minegishi H., Usami R., Ventosa A.. 2011; A multilocus sequence analysis approach to the phylogeny and taxonomy of the Halobacteriales . Int J Syst Evol Microbiol61:2984–2995 [CrossRef][PubMed]
    [Google Scholar]
  58. Papke R. T., Corral P., Ram-Mohan N., Haba R. R., Sánchez-Porro C., Makkay A., Ventosa A.. 2015; Horizontal gene transfer, dispersal and haloarchaeal speciation. Life (Basel)5:1405–1426[PubMed]
    [Google Scholar]
  59. Parte A. C.. 2015; List of Prokaryotic Names with Standing in Nomenclature. http://www.bacterio.net
  60. Pesenti P. T., Sikaroodi M., Gillevet P. M., Sánchez-Porro C., Ventosa A., Litchfield C. D.. 2008; Halorubrum californiense sp. nov., an extreme archaeal halophile isolated from a crystallizer pond at a solar salt plant in California, USA. Int J Syst Evol Microbiol58:2710–2715 [CrossRef][PubMed]
    [Google Scholar]
  61. Ram-Mohan N., Fullmer M. S., Makkay A. M., Wheeler R., Ventosa A., Naor A., Gogarten J. P., Papke R. T.. 2014; Evidence from phylogenetic and genome fingerprinting analyses suggests rapidly changing variation in Halorubrum and Haloarcula populations. Front Microbiol5:143[PubMed][CrossRef]
    [Google Scholar]
  62. Rodríguez-Valera F., Ruiz-Berraquero F., Ramos-Cormenzana A.. 1980; Isolation of extremely halophilic bacteria able to grow in defined inorganic media with single carbon sources. J Gen Microbiol119:535–538
    [Google Scholar]
  63. Roh S. W., Bae J. W.. 2009; Halorubrum cibi sp. nov., an extremely halophilic archaeon from salt-fermented seafood. J Microbiol47:162–166 [CrossRef][PubMed]
    [Google Scholar]
  64. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425[PubMed]
    [Google Scholar]
  65. Sambrook J., Russell D. W.. editors 2001; Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  66. Smibert R. M., Krieg N. R.. 1981; General characterization. In Manual of Methods for General Bacteriology pp409–443Edited by Gerhardt P., Murray R. G. E., Costilow R. N., Nester E. W., Wood W. A., Krieg N. R., Phillips G. B.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  67. Stackebrandt E., Goebel B. M.. 1994; Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol44:846–849 [CrossRef]
    [Google Scholar]
  68. Stackebrandt E., Frederiksen W., Garrity G. M., Grimont P. A. D., Kämpfer P., Maiden M. C. J., Nesme X., Rosselló-Mora R., Swings J., other authors. 2002; Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int Syst Evol Microbiol52:1043–1047[PubMed]
    [Google Scholar]
  69. Stamatakis A., Ludwig T., Meier H.. 2005; RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics21:456–463 [CrossRef][PubMed]
    [Google Scholar]
  70. Subow N. N.. 1931; Oceanographical Tables Moscow: Oceanographical Institute of USSR, Commissariat of Agriculture of USSR, Hydro-Meteorological Committee of USSR (in Russian);
    [Google Scholar]
  71. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol28:2731–2739 [CrossRef][PubMed]
    [Google Scholar]
  72. Ventosa A., Gutiérrez M. C., Kamekura M., Dyall-Smith M. L.. 1999; Proposal to transfer Halococcus turkmenicus, Halobacterium trapanicum JCM 9743 and strain GSL-11 to Haloterrigena turkmenica gen. nov., comb. nov. Int J Syst Bacteriol49:131–136 [CrossRef][PubMed]
    [Google Scholar]
  73. Walsh D. A., Bapteste E., Kamekura M., Doolittle W. F.. 2004; Evolution of the RNA polymerase B′ subunit gene (rpoB′) in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. Mol Biol Evol21:2340–2351 [CrossRef][PubMed]
    [Google Scholar]
  74. Wayne L. G., Brenner D. J., Colwell R. R., Grimont P. A. D., Kandler O., Krichevsky M. I., Moore L. H., Moore W. E. C., Murray R. G. E., other authors. 1987; Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol37:463–464[CrossRef]
    [Google Scholar]
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