1887

Abstract

A polyphasic comparative taxonomic study of Halorubrum ezzemoulense Kharroub et al. 2006, Halorubrum chaoviator Mancinelli et al. 2009 and eight new Halorubrum strains related to these haloarchaeal species was carried out. Multilocus sequence analysis using the five concatenated housekeeping genes atpB, EF-2, glnA, ppsA and rpoB′, and phylogenetic analysis based on the 757 core protein sequences obtained from their genomes showed that Hrr. ezzemoulense DSM 17463, Hrr. chaoviator Halo-G* (=DSM 19316) and the eight Halorubrum strains formed a robust cluster, clearly separated from the remaining species of the genus Halorubrum . The orthoANI value and digital DNA–DNA hybridization value, calculated by the Genome-to-Genome Distance Calculator (GGDC), showed percentages among Hrr. ezzemoulense DSM 17463, Hrr. chaoviator DSM 19316 and the eight Halorubrum strains ranging from 99.4 to 97.9 %, and from 95.0 to 74.2 %, respectively, while these values for those strains and the type strains of the most closely related species of Halorubrum were 88.7–77.4 % and 36.1–22.3 %, respectively. Although some differences were observed, the phenotypic and polar lipid profiles were quite similar for all the strains studied. Overall, these data show that Hrr. ezzemoulense, Hrr. chaoviator and the eight new Halorubrum isolates constitute a single species. Thus, Hrr. chaoviator should be considered as a later, heterotypic synonym of Hrr. ezzemoulense . We propose an emended description of Hrr. ezzemoulense , including the features of Hrr. chaoviator and those of the eight new isolates.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003005
2018-09-14
2024-10-13
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/68/11/3657.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.003005&mimeType=html&fmt=ahah

References

  1. Gupta RS, Naushad S, Baker S. Phylogenomic analyses and molecular signatures for the class Halobacteria and its two major clades: a proposal for division of the class Halobacteria into an emended order Halobacteriales and two new orders, Haloferacales ord. nov. and Natrialbales ord. nov., containing the novel families Haloferacaceae fam. nov. and Natrialbaceae fam. nov. Int J Syst Evol Microbiol 2015; 65:1050–1069 [View Article][PubMed]
    [Google Scholar]
  2. Gupta RS, Naushad S, Fabros R, Adeolu M. A phylogenomic reappraisal of family-level divisions within the class Halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie van Leeuwenhoek 2016; 109:565–587 Erratum: Antonie van Leeuwenhoek 2016;109:1521-1523 [View Article][PubMed]
    [Google Scholar]
  3. 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]
  4. Amoozegar MA, Siroosi M, Atashgahi S, Smidt H, Ventosa A. Systematics of haloarchaea and biotechnological potential of their hydrolytic enzymes. Microbiology 2017; 163:623–645 [View Article][PubMed]
    [Google Scholar]
  5. Ram Mohan N, Fullmer MS, Makkay AM, Wheeler R, Ventosa A et al. Evidence from phylogenetic and genome fingerprinting analyses suggests rapidly changing variation in Halorubrum and Haloarcula populations. Front Microbiol 2014; 5:143 [View Article][PubMed]
    [Google Scholar]
  6. Fullmer MS, Soucy SM, Swithers KS, Makkay AM, Wheeler R et al. Population and genomic analysis of the genus Halorubrum. Front Microbiol 2014; 5:140 [View Article][PubMed]
    [Google Scholar]
  7. de la Haba RR, Corral P, Sánchez-Porro C, Infante-Domínguez C, Makkay AM et al. Genotypic and lipid analyses of strains from the archaeal genus Halorubrum reveal insights into their taxonomy, divergence, and population structure. Front Microbiol 2018; 9:512 [View Article][PubMed]
    [Google Scholar]
  8. Kharroub K, Quesada T, Ferrer R, Fuentes S, Aguilera M et al. Halorubrum ezzemoulense sp. nov., a halophilic archaeon isolated from Ezzemoul sabkha, Algeria. Int J Syst Evol Microbiol 2006; 56:1583–1588 [View Article][PubMed]
    [Google Scholar]
  9. Mancinelli RL, Landheim R, Sánchez-Porro C, Dornmayr-Pfaffenhuemer M, Gruber C et al. Halorubrum chaoviator sp. nov., a haloarchaeon isolated from sea salt in Baja California, Mexico, Western Australia and Naxos, Greece. Int J Syst Evol Microbiol 2009; 59:1908–1913 [View Article][PubMed]
    [Google Scholar]
  10. Rodríguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A. Isolation of extremely halophilic bacteria able to grow in defined inorganic media with single carbon sources. J Gen Microbiol 1980; 119:535–538 [View Article]
    [Google Scholar]
  11. Subov NN. Oceanographical Tables Moscow: Commissariat of Agriculture of USSR, Hydro-Meteorological Committee of USSR and Oceanographical Institute of USSR; 1931
    [Google Scholar]
  12. 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 [View Article][PubMed]
    [Google Scholar]
  13. Yoon SH, Ha SM, 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; 67:1614–1617 [View Article][PubMed]
    [Google Scholar]
  14. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article][PubMed]
    [Google Scholar]
  15. Kluge AG, Farris JS. Quantitative phyletics and the evolution of anurans. Syst Zool 1969; 18:1–32 [View Article]
    [Google Scholar]
  16. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article][PubMed]
    [Google Scholar]
  17. Posada D. Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics 2003; Chapter 6:6.5.1–6.5.6 [View Article][PubMed]
    [Google Scholar]
  18. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article][PubMed]
    [Google Scholar]
  19. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  20. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016:e1900v1
    [Google Scholar]
  21. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [View Article][PubMed]
    [Google Scholar]
  22. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 1992; 8:275–282 [View Article][PubMed]
    [Google Scholar]
  23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  24. 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]
  25. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  26. Auch AF, von Jan M, Klenk HP, 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]
  27. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  28. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014; 64:316–324 [View Article][PubMed]
    [Google Scholar]
  29. 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]
  30. Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 2016; 66:1100–1103 [View Article][PubMed]
    [Google Scholar]
  31. Oren A, Ventosa A, Grant WD. Proposed minimal standards for desciption of new taxa in the order Halobacteriales. Int J Syst Bacteriol 1997; 47:233–238 [View Article]
    [Google Scholar]
  32. Dussault HP. An improved technique for staining red halophilic bacteria. J Bacteriol 1955; 70:484–485[PubMed]
    [Google Scholar]
  33. Corral P, de la Haba RR, Sánchez-Porro C, Ali Amoozegar M, Thane Papke R et al. Halorubrum halodurans sp. nov., an extremely halophilic archaeon isolated from a hypersaline lake. Int J Syst Evol Microbiol 2016; 66:435–444 [View Article][PubMed]
    [Google Scholar]
  34. Barrow GI, Feltham RKA. Cowan Steel’s Manual for the Identification of Medical Bacteria, 3rd ed. Cambridge: Cambridge University Press; 2003
    [Google Scholar]
  35. Gerhardt P, Murray RGE, Woo WA, Krieg NR. Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1994
    [Google Scholar]
  36. Smibert RM, Krieg NR. General characterization. In Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA et al. (editors) Methods for General and Molecular Bacteriology Washington, DC: American Society for Microbiology; 1981 pp. 409–443
    [Google Scholar]
  37. Ventosa A, Quesada E, Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A. Numerical taxonomy of moderately halophilic Gram-negative rods. Microbiology 1982; 128:1959–1968 [View Article]
    [Google Scholar]
  38. Corcelli A, Lobasso S. Characterization of lipids of halophilic archaea. Methods Microbiol 2006; 35:585–613
    [Google Scholar]
  39. Angelini R, Corral P, Lopalco P, Ventosa A, Corcelli A. Novel ether lipid cardiolipins in archaeal membranes of extreme haloalkaliphiles. Biochim Biophys Acta 2012; 1818:1365–1373 [View Article][PubMed]
    [Google Scholar]
  40. Corral P, de la Haba RR, Sánchez-Porro C, Amoozegar MA, Papke RT et al. Halorubrum persicum sp. nov., an extremely halophilic archaeon isolated from sediment of a hypersaline lake. Int J Syst Evol Microbiol 2015; 65:1770–1778 [View Article][PubMed]
    [Google Scholar]
  41. Kates M. Techniques of lipidology: isolation, analysis and identification of lipids. In Burdon RH, van Knippenberg PH. (editors) Laboratory Techniques in Biochemistry and Molecular Biology Amsterdam: Elsevier; 1986 pp. 100–110
    [Google Scholar]
  42. Fuchs B, Schiller J, Süss R, Schürenberg M, Suckau D. 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 Chem 2007; 389:827–834 [View Article][PubMed]
    [Google Scholar]
  43. Kean EL. Rapid, sensitive spectrophotometric method for quantitative determination of sulfatides. J Lipid Res 1968; 9:319–327[PubMed]
    [Google Scholar]
  44. McGenity TJ, Grant WD. 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 Microbiol 1995; 18:237–243 [View Article]
    [Google Scholar]
  45. Oren A, Arahal DR, Ventosa A. Emended descriptions of genera of the family Halobacteriaceae. Int J Syst Evol Microbiol 2009; 59:637–642 [View Article][PubMed]
    [Google Scholar]
  46. Parker CT, Tindall BJ, Garrity GM. International Code of Nomenclature of Prokaryotes. Int J Syst Evol Microbiol 2015 [View Article][PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.003005
Loading
/content/journal/ijsem/10.1099/ijsem.0.003005
Loading

Data & Media loading...

Supplements

Supplementary File 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