Marinococcus salis sp., nov., a moderately halophilic bacterium isolated from a salt marsh

Abstract

A novel Gram-stain-positive, coccoid-shaped, facultative anaerobic, motile and halophilic bacterium strain 5MT was isolated from Surajbari in India. Based on the 16S rRNA gene sequence analysis, it was identified as belonging to the genus Marinococcus and was most closely related to Marinococcus luteus KCTC 13214T (99.3 %, sequence similarity), Marinococcus halotolerans KCTC 19045T (99.0 %), Marinococcus halophilus LMG 17439T (98.8 %) and Marinococcus tarijensis LMG 26930T (98.7 %). However, the DNA–DNA relatedness of strain 5MT with M. luteus KCTC 13214T, M. halotolerans KCTC 19045T, M. halophilus LMG 17439T and M. tarijensis LMG 26930T was 42.6 ± 0.8, 48.6 ± 0.8, 40.9 ± 0.8 and 39.8 ± 0.9 %, respectively. Strain 5MT grows optimally at 5 % (w/v) NaCl, pH 7.5–8.5 and 37 °C. The cell-wall peptidoglycan of strain 5MT contains meso-diaminopimelic acid. Polar lipids of the strain 5MT include diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, a phospholipid and two unknown lipids. The predominant isoprenoid quinone was MK-7. DNA G+C content was 48.9 mol%, and anteiso-C15:0 (40.9 %) was the predominant fatty acid. The results of phylogenetic, biochemical tests and chemotaxonomic allowed a clear differentiation of strain 5MT from all of its nearest phylogenetic neighbours, which represents a novel member of the genus Marinococcus, for which the name Marinococcus salis sp., nov., is proposed. The type strain is 5MT (=KCTC 33743T = LMG 29101T = CGMCC 1.15385T).

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Arahal DR, Ventosa A (2002) Moderately halophilic and halotolerant species of Bacillus and related genera. In: Berkeley R, Heyndrickx M, Logan N, De Vos P (eds) Applications and systematics of Bacillus and relatives. Blackwell, Oxford, pp 83–99

    Chapter  Google Scholar 

  2. Balderrama-Subieta A, Guzmán D, Minegishi H, Echigo A, Shimane Y, Hatada Y, Quillaguamán J (2013) Marinococcus tarijensis sp. nov., a moderately halophilic bacterium isolated from a salt mine. Int J Syst Evol Microbiol 63:3319–3323

    CAS  Article  PubMed  Google Scholar 

  3. Hao MV, Kocur M, Komogata K (1984) Marinococcus gen. nov., a new genus for motile cocci with meso-diaminopimelic acid in the cell wall; and Marinococcus albus sp. nov. and Marinococcus halophilus (Novitsky and Kushner) comb. nov. J Gen Appl Microbiol 30:449–459

    Article  Google Scholar 

  4. Hasegawa T, Takizaea M, Tanida S (1983) A rapid analysis for chemical grouping of aerobic actinomycetes. J Gen Appl Microbiol 29:319–322

    CAS  Article  Google Scholar 

  5. Kates M (1972) Techniques of lipidology. Elsevier, New York

    Book  Google Scholar 

  6. Kates M (1986) Techniques of lipidology: isolation, analysis, and identification of lipids. Elsevier, Amsterdam

    Google Scholar 

  7. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    CAS  Article  PubMed  Google Scholar 

  8. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  Article  PubMed  Google Scholar 

  9. Li W-J, Schumann P, Zhang Y-Q, Chen G-Z, Tian X-P, Xu L-H, Stackebrandt E, Jiang C-L (2005) Marinococcus halotolerans sp. nov., isolated from Qinghai, North-West China. Int J Syst Evol Microbiol 55:1801–1804

    CAS  Article  PubMed  Google Scholar 

  10. Logan NA, Berge O, Bishop AH, Busse H-J, De Vos P, Fritze D et al (2009) Proposed minimal standards for describing new taxa of aerobic, endospore forming bacteria. Int J Syst Evol Microbiol 59:2114–2121

    CAS  Article  PubMed  Google Scholar 

  11. Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218

    CAS  Article  Google Scholar 

  12. Marquez MC, Ventosa A, Ruiz-Berraquero F (1990) Marinococcus hispanicus, a new species of moderately halophilic Gram-positive cocci. Int J Syst Bacteriol 40:165–169

    Article  Google Scholar 

  13. Meier-Kolthoff JP, Gӧker M, Sprӧer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418

    CAS  Article  PubMed  Google Scholar 

  14. Mesbah M, Premachandran U, Whitman WB (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39:159–167

    CAS  Article  Google Scholar 

  15. Novitsky TJ, Kushner DJ (1976) Planococcus halophilus sp. nov., a facultatively halophilic coccus. Int J Syst Bacteriol 26:53–57

    Article  Google Scholar 

  16. Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63

    CAS  Article  PubMed  Google Scholar 

  17. Oren A, Duker S, Ritter S (1996) The polar lipid composition of Walsby’s square bacterium. FEMS Microbiol Lett 138:135–140

    CAS  Article  Google Scholar 

  18. Parte AC (2016) List of prokaryotic names with standing in nomenclature. http://www.bacterio.net

  19. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Inc, Newark

    Google Scholar 

  20. Schleifer KH (1985) Analysis of the chemical composition and primary structure of murein. Methods Microbiol 18:123–156

    CAS  Article  Google Scholar 

  21. Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Smibert RM, Krieg NR (1981) General characterization. In: Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (eds) Manual of methods for general microbiology. American Society for Microbiology, Washington, pp 409–443

    Google Scholar 

  23. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P (ed) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654

    Google Scholar 

  24. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 4:152–155

    Google Scholar 

  25. Stackebrandt E, Goebel BM (1994) Place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849

    CAS  Article  Google Scholar 

  26. Tamaoka J, Fujimura Y-K, Kuraishi H (1983) Analysis of bacterial menaquinone mixtures by high performance liquid chromatography. J Appl Microbiol 54:31–36

    CAS  Google Scholar 

  27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Tindall BJ (1990a) Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66:199–202

    CAS  Article  Google Scholar 

  29. Tindall BJ (1990b) A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 13:128–130

    CAS  Article  Google Scholar 

  30. Tourova TP, Antonov AS (1987) Identification of microorganisms by rapid DNA–DNA hybridization. Methods Microbiol 19:333–355

    Article  Google Scholar 

  31. Ventosa A (2006) Unusual micro-organisms from unusual habitats: hypersaline environments. In: Logan NA, Lappin-Scott HM, Oyston PCF (eds) Prokaryotic diversity: mechanisms and significance. Cambridge University Press, Cambridge, pp 223–254

    Chapter  Google Scholar 

  32. Ventosa A, Quesada E, Rodriguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1982) Numerical taxonomy of moderately halophilic Gram-negative rods. J Gen Microbiol 128:1959–1968

    Google Scholar 

  33. Ventosa A, Marquez MC, Weiss N, Tindall BJ (1992) Transfer of Marinococcus hispanicus to the genus Salinicoccus as Salinicoccus hispanicus comb. nov. Syst Appl Microbiol 15:530–534

    Article  Google Scholar 

  34. Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Vishnuvardhan Reddy S, Aspana S, Tushar DL, Sasikala CH, Ramana V (2013) Spirochaeta sphaeroplastigenens sp. nov., a halo-alkaliphilic, obligately anaerobic spirochaete isolated from soda lake Lonar. Int J Syst Evol Microbiol 63:2223–2228

    Article  PubMed  Google Scholar 

  36. Wang Y, Cao L-L, Tang S-K, Lou K, Mao P-H, Jin X, Jiang C-L, Xu L-H, Li W-J (2009) Marinococcus luteus sp. nov., a halotolerant bacterium isolated from a salt lake, and emended description of the genus Marinococcus. Int J Syst Evol Microbiol 59:2875–2879

    CAS  Article  PubMed  Google Scholar 

  37. Yoon JH, Kang SJ, Oh TK (2007) Reclassification of Marinococcus albus. Int J Syst Evol Microbiol 57:2406–2411

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

S.V.R. and M.T. thank Department of Science and Technology, Government of India, for providing FTSYS Project Grants (SB/FT/LS-115/2012 and SB/FT/LS-320/2012, respectively). M.F. also thanks DST for PA fellowship.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sultanpuram Vishnuvardhan Reddy.

Additional information

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequences of strain 5MT is LN879357.

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Two-dimensional thin-layer chromatogram of polar lipid extracts of strain 5MT and related Marinococcus species. The first direction was developed in CHCl3:CH3OH:H2O (75:32:4 by volume) and the second in CHCl3:CH3OH:CH3COOH:H2O (86:16:15:4 by volume). PG, phosphatidylglycerol; DPG, diphosphatidylglycerol; PE, phosphatidylethanolamine; PL1, unknown phospholipid; and L1-7, unknown lipids (PDF 437 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vishnuvardhan Reddy, S., Thirumala, M., Farooq, M. et al. Marinococcus salis sp., nov., a moderately halophilic bacterium isolated from a salt marsh. Arch Microbiol 198, 1013–1018 (2016). https://doi.org/10.1007/s00203-016-1263-z

Download citation

Keywords

  • Marinococcus salis sp. nov.
  • Polyphasic taxonomy
  • Moderate halophile