1887

Abstract

A novel halophilic bacterium, strain 71-i, was isolated from Inche-Broun hypersaline lake in Golestan province, in the north of Iran. It was a Gram-stain-negative, non-endospore forming, rod-shaped bacterium. It grew at 4–40 °C (optimum 30 °C), pH 6.0–11.0 (optimum pH 7.5) and with 0.5–15 % (w/v) NaCl [optimum 3 % (w/v) NaCl]. The results of phylogenetic analyses based on the 16S rRNA gene sequence comparison indicated its affiliation to the genus and the low percentage of identity with the most closely related species (97.5 %), indicated its placement as a novel species within this genus. Digital DNA–DNA hybridization (dDDH) values and average nucleotide identity (ANI) analyses of this strain against closely related species confirmed its condition of novel taxon. On the other hand, the percentage of the average amino acid identity (AAI) affiliated strain 71-i within the genus . The DNA G+C content of this isolate was 57.7 mol%. The major fatty acids were C and Cω and/or C ω6. Ubiquinone-9 was the major isoprenoid quinone and diphosphatidylglycerol (DPG), phosphatidylglycerol (PG) and phosphatidylethanolamine (PE) were the main polar lipids of this strain. On the basis of the phylogenomic and phenotypic (including chemotaxonomic) features, we propose strain 71-i (= IBRC M 11023 = CECT 30160 = LMG 29252) as the type strain of a novel species within the genus , with the name sp. nov. Genomic detections of this strain in various metagenomic databases indicate that it is a relatively abundant species in environments with low salinities (approximately 5 % salinity), but not in hypersaline habitats with high salt concentrations.

Funding
This study was supported by the:
  • MCIN/AEI/10.13039/501100011033 (Award PID2020-118136GB-I00)
    • Principle Award Recipient: NotApplicable
  • Iranian National Science Foundation (INSF) (MAA).
    • Principle Award Recipient: NotApplicable
  • Research Council of the University of Tehran
    • Principle Award Recipient: NotApplicable
  • Consejería de Conocimiento, Investigación y Universidad, Junta de Andalucía (Award P20_01066 and BIO-213)
    • Principle Award Recipient: AntonioVentosa
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006083
2023-10-27
2024-06-15
Loading full text...

Full text loading...

References

  1. 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 [View Article] [PubMed]
    [Google Scholar]
  2. Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M et al. Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 1992; 42:568–576 [View Article] [PubMed]
    [Google Scholar]
  3. Liao H, Lin X, Li Y, Qu M, Tian Y. Reclassification of the taxonomic framework of orders Cellvibrionales, Oceanospirillales, Pseudomonadales, and Alteromonadales in class Gammaproteobacteria through phylogenomic tree analysis. mSystems 2020; 5:e00543-20 [View Article] [PubMed]
    [Google Scholar]
  4. Tindall BJ. Marinobacter nauticus (Baumann et al. 1972) comb. nov. arising from instances of synonymy and the incorrect interpretation of the International Code of Nomenclature of Prokaryotes. Arch Microbiol 2020; 202:657–663 [View Article] [PubMed]
    [Google Scholar]
  5. 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]
  6. León MJ, Sánchez-Porro C, Ventosa A. Marinobacter aquaticus sp. nov., a moderately halophilic bacterium from a solar saltern. Int J Syst Evol Microbiol 2017; 67:2622–2627 [View Article] [PubMed]
    [Google Scholar]
  7. Cui Z, Gao W, Xu G, Luan X, Li Q et al. Marinobacter aromaticivorans sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from sea sediment. Int J Syst Evol Microbiol 2016; 66:353–359 [View Article] [PubMed]
    [Google Scholar]
  8. Romanenko LA, Schumann P, Rohde M, Zhukova NVM. Marinobacter bryozoorum sp. nov. and Marinobacter sediminum sp. nov., novel bacteria from the marine environment. Int J Syst Evol Microbiol 2005; 55:143–148 [View Article] [PubMed]
    [Google Scholar]
  9. Yoon J-H, Yeo S-H, Kim I-G, Oh T-K. Marinobacter flavimaris sp. nov. and Marinobacter daepoensis sp. nov., slightly halophilic organisms isolated from sea water of the Yellow Sea in Korea. Int J Syst Evol Microbiol 2004; 54:1799–1803 [View Article] [PubMed]
    [Google Scholar]
  10. Rani S, Koh H-W, Kim H, Rhee S-K, Park S-J. Marinobacter salinus sp. nov., a moderately halophilic bacterium isolated from a tidal flat environment. Int J Syst Evol Microbiol 2017; 67:205–211 [View Article] [PubMed]
    [Google Scholar]
  11. Zhong Z-P, Liu Y, Liu H-C, Wang F, Zhou Y-G et al. Marinobacter halophilus sp. nov., a halophilic bacterium isolated from a salt lake. Int J Syst Evol Microbiol 2015; 65:2838–2845 [View Article] [PubMed]
    [Google Scholar]
  12. Bagheri M, Amoozegar MA, Didari M, Makhdoumi-Kakhki A, Schumann P et al. Marinobacter persicus sp. nov., a moderately halophilic bacterium from a saline lake in Iran. Antonie van Leeuwenhoek 2013; 104:47–54 [View Article] [PubMed]
    [Google Scholar]
  13. Kaeppel EC, Gärdes A, Seebah S, Grossart H-P, Ullrich MS. Marinobacter adhaerens sp. nov., isolated from marine aggregates formed with the diatom Thalassiosira weissflogii. Int J Syst Evol Microbiol 2012; 62:124–128 [View Article] [PubMed]
    [Google Scholar]
  14. Green DH, Bowman JP, Smith EA, Gutierrez T, Bolch CJS. Marinobacter algicola sp. nov., isolated from laboratory cultures of paralytic shellfish toxin-producing dinoflagellates. Int J Syst Evol Microbiol 2006; 56:523–527 [View Article] [PubMed]
    [Google Scholar]
  15. Yang Q, Feng Q, Zhang B-P, Gao J-J, Sheng Z et al. Marinobacter alexandrii sp. nov., a novel yellow-pigmented and algae growth-promoting bacterium isolated from marine phycosphere microbiota. Antonie van Leeuwenhoek 2021; 114:709–718 [View Article] [PubMed]
    [Google Scholar]
  16. Lee OO, Lai PY, Wu H-X, Zhou X-J, Miao L et al. Marinobacter xestospongiae sp. nov., isolated from the marine sponge Xestospongia testudinaria collected from the Red Sea. Int J Syst Evol Microbiol 2012; 62:1980–1985 [View Article] [PubMed]
    [Google Scholar]
  17. Yi E, Shao Z, Li G, Liang X, Zhou M. Marinobacter mangrovi sp. nov., isolated from mangrove sediment. Int J Syst Evol Microbiol 2021; 71:5079 [View Article] [PubMed]
    [Google Scholar]
  18. Handley KM, Héry M, Lloyd JR. Marinobacter santoriniensis sp. nov., an arsenate-respiring and arsenite-oxidizing bacterium isolated from hydrothermal sediment. Int J Syst Evol Microbiol 2009; 59:886–892 [View Article] [PubMed]
    [Google Scholar]
  19. Liu C, Chen C-X, Zhang X-Y, Yu Y, Liu A et al. Marinobacter antarcticus sp. nov., a halotolerant bacterium isolated from Antarctic intertidal sandy sediment. Int J Syst Evol Microbiol 2012; 62:1838–1844 [View Article] [PubMed]
    [Google Scholar]
  20. Zhang M-X, Li A-Z, Wu Q, Yao Q, Zhu H-H. Marinobacter denitrificans sp. nov., isolated from marine sediment of southern Scott Coast, Antarctica. Int J Syst Evol Microbiol 2020; 70:2918–2924 [View Article] [PubMed]
    [Google Scholar]
  21. Montes MJ, Bozal N, Mercadé E. Marinobacter guineae sp. nov., a novel moderately halophilic bacterium from an Antarctic environment. Int J Syst Evol Microbiol 2008; 58:1346–1349 [View Article] [PubMed]
    [Google Scholar]
  22. Zhang D-C, Li H-R, Xin Y-H, Chi Z-M, Zhou P-J et al. Marinobacter psychrophilus sp. nov., a psychrophilic bacterium isolated from the Arctic. Int J Syst Evol Microbiol 2008; 58:1463–1466 [View Article] [PubMed]
    [Google Scholar]
  23. Liebgott P-P, Casalot L, Paillard S, Lorquin J, Labat M. Marinobacter vinifirmus sp. nov., a moderately halophilic bacterium isolated from a wine-barrel-decalcification wastewater. Int J Syst Evol Microbiol 2006; 56:2511–2516 [View Article] [PubMed]
    [Google Scholar]
  24. Tinker K, Lipus D, Gardiner J, Stuckman M, Gulliver D. The microbial community and functional potential in the Midland Basin reveal a community dominated by both thiosulfate and sulfate-reducing microorganisms. Microbiol Spectr 2022; 10:e0004922 [View Article] [PubMed]
    [Google Scholar]
  25. Nosalova L, Piknova M, Bonova K, Pristas P. Deep subsurface hypersaline environment as a source of novel species of halophilic sulfur-oxidizing bacteria. Microorganisms 2022; 10:995 [View Article] [PubMed]
    [Google Scholar]
  26. Deng Y, Wang K, Hu Z, Tang Y-Z. Abundant species diversity and essential functions of bacterial communities associated with dinoflagellates as revealed from metabarcoding sequencing for laboratory-raised clonal cultures. Int J Environ Res Public Health 2022; 19:4446 [View Article] [PubMed]
    [Google Scholar]
  27. Abramov SM, Straub D, Tejada J, Grimm L, Schädler F et al. Biogeochemical niches of Fe-cycling communities influencing heavy metal transport along the Rio Tinto, Spain. Appl Environ Microbiol 2022; 88:e0229021 [View Article] [PubMed]
    [Google Scholar]
  28. Rasooli M, Amoozegar MA, Akhavan Sepahy A, Babavalian H, Tebyanian H. Isolation, identification and extracellular enzymatic activity of culturable extremely halophilic archaea and bacteria of IncheBoroun Wetland. Int Lett Nat Sci 2016; 56:40–51 [View Article]
    [Google Scholar]
  29. Marmur J. A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 1961; 3:208–218 [View Article]
    [Google Scholar]
  30. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, III Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press; 2001
    [Google Scholar]
  31. Lane DJ. 16S/23S rRNA sequencing. In Stackebrandt E, Goodfellow M. eds Nucleic Acid Techniques in Bacterial Systematics Chichester: Wiley; 1991 pp 115–175
    [Google Scholar]
  32. 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; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  33. 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]
  34. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol 1971; 20:406–416 [View Article]
    [Google Scholar]
  35. 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]
  36. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  37. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  38. Ng HJ, Lopez-Perez M, Webb HK, Gomez D, Sawabe T et al. Marinobacter salarius sp. nov. and Marinobacter similis sp. nov., isolated from sea water. PLoS One 2014; 9:e106514 [View Article]
    [Google Scholar]
  39. Gu J, Cai H, Yu S-L, Qu R, Yin B et al. Marinobacter gudaonensis sp. nov., isolated from an oil-polluted saline soil in a Chinese oilfield. Int J Syst Evol Microbiol 2007; 57:250–254 [View Article] [PubMed]
    [Google Scholar]
  40. Zhang Y, Zhong X-C, Xu W, Lu D-C, Zhao J-X et al. Marinobacter vulgaris sp. nov., a moderately halophilic bacterium isolated from a marine solar saltern. Int J Syst Evol Microbiol 2020; 70:450–456 [View Article]
    [Google Scholar]
  41. Verma A, Mual P, Mayilraj S, Krishnamurthi S. Tamilnaduibacter salinus gen. nov., sp. nov., a halotolerant gammaproteobacterium within the family Alteromonadaceae, isolated from a salt pan in Tamilnadu, India. Int J Syst Evol Microbiol 2015; 65:3248–3255 [View Article] [PubMed]
    [Google Scholar]
  42. Liao H, Li Y, Guo X, Lin X, Lai Q et al. Mangrovitalea sediminis gen. nov., sp. nov., a member of the family Alteromonadaceae isolated from mangrove sediment. Int J Syst Evol Microbiol 2017; 67:5172–5178 [View Article] [PubMed]
    [Google Scholar]
  43. 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 [View Article] [PubMed]
    [Google Scholar]
  44. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  45. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  46. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  47. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  48. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5:113 [View Article] [PubMed]
    [Google Scholar]
  49. Price MN, Dehal PS, Arkin AP. FastTree 2 — approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  50. Lee I, Ouk Kim Y, Park S-C, 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]
  51. 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 [View Article] [PubMed]
    [Google Scholar]
  52. Auch AF, Klenk H-P, Göker M. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand Genomic Sci 2010; 2:142–148 [View Article] [PubMed]
    [Google Scholar]
  53. 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]
  54. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 2005; 102:2567–2572 [View Article] [PubMed]
    [Google Scholar]
  55. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article] [PubMed]
    [Google Scholar]
  56. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 1994; 44:846–849 [View Article]
    [Google Scholar]
  57. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  58. 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]
  59. Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J 2017; 11:2399–2406 [View Article] [PubMed]
    [Google Scholar]
  60. Murray R. Determinative and cytological light microscopy. In Methods for General and Molecular Bacteriology 1994 pp 7–20
    [Google Scholar]
  61. Krieg NR, Padgett PJ. Phenotypic and physiological characterization methods. In Methods in Microbiology Elsevier; 2011 pp 15–60
    [Google Scholar]
  62. Gutiérrez C, González C. Method for simultaneous detection of proteinase and esterase activities in extremely halophilic bacteria. Appl Microbiol 1972; 24:516–517 [View Article] [PubMed]
    [Google Scholar]
  63. Mata JA, Martínez-Cánovas J, Quesada E, Béjar V. A detailed phenotypic characterisation of the type strains of Halomonas species. Syst Appl Microbiol 2002; 25:360–375 [View Article] [PubMed]
    [Google Scholar]
  64. Leifson E. Determination of carbohydrate metabolism of marine bacteria. J Bacteriol 1963; 85:1183–1184 [View Article]
    [Google Scholar]
  65. 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]
  66. Mueller JH, Hinton J. A protein-free medium for primary isolation of the gonococcus and meningococcus. Exp Biol Med 1941; 48:330–333 [View Article]
    [Google Scholar]
  67. Kämpfer P, Kroppenstedt RM. Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 1996; 42:989–1005 [View Article]
    [Google Scholar]
  68. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al. An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 1984; 2:233–241 [View Article]
    [Google Scholar]
  69. Ghai R, Pašić L, Fernández AB, Martin-Cuadrado A-B, Mizuno CM et al. New abundant microbial groups in aquatic hypersaline environments. Sci Rep 2011; 1:135 [View Article] [PubMed]
    [Google Scholar]
  70. Fernández AB, Ghai R, Martin-Cuadrado A-B, Sánchez-Porro C, Rodriguez-Valera F et al. Prokaryotic taxonomic and metabolic diversity of an intermediate salinity hypersaline habitat assessed by metagenomics. FEMS Microbiol Ecol 2014; 88:623–635 [View Article] [PubMed]
    [Google Scholar]
  71. Naghoni A, Emtiazi G, Amoozegar MA, Cretoiu MS, Stal LJ et al. Microbial diversity in the hypersaline Lake Meyghan, Iran. Sci Rep 2017; 7:11522 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.006083
Loading
/content/journal/ijsem/10.1099/ijsem.0.006083
Loading

Data & Media loading...

Supplements

Supplementary material 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