Skip to main content
SpringerLink
Log in

Halomonas sambharensis sp. nov., a Moderately Halophilic Bacterium Isolated from the Saltern Crystallizer Ponds of the Sambhar Salt Lake in India

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Two moderately halophilic strains SBS 10T and SSO 06 were isolated from the saltern crystallizer ponds of the hypersaline Sambhar Salt Lake in India. Strains were aerobic, Gram-stain-negative, and rod shaped. Phylogenetic analysis based on the 16S rRNA gene sequences indicated that two strains belong to the genus Halomonas in the Gammaproteobacteria, with highest 16S rRNA gene sequence similarities with Halomonas gudaonensis LMG 23610T (98.2% similarity) and Halomonas campaniensis 5AGT (99.0% similarity). Strains grew optimally at 37 °C, pH 7.5–8.0 in the presence of 5–8% (w/v) NaCl. The major fatty acids of the strain SBS 10T were C18:1ω7c (54.37%), C16:0 (25.69%), C16:1 × 7c/C16:1 × 6c (13.28%), and C12:0 (1.21%). The G+C content was 63.6 mol % (Tm). Phenotypic features, fatty acids profile, and DNA G+C content supported placement of the strain SBS 10T in the genus Halomonas having distinct characteristics with related strains. Analysis of the housekeeping genes: gryB and rpoD and in silico DNA-DNA hybridization between the strain SBS 10T and its type strain Halomonas gudaonensis (LMG 23610T) further revealed the strain SBS 10T to be a distinct species. On the basis of the phenotypic, chemotaxonomic and phylogenetic analysis, the strain SBS 10T is considered to represent a novel species for which the name Halomonas sambharensis is proposed. The type strain is SBS 10T (= MTCC 12313T = LMG 30344T).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Reddy G, Raghavan P, Sarita N, Prakash J, Nagesh N, Delille D, Shivaji S (2003) Halomonas glaciei sp. nov. isolated from fast ice of adelie land, antarctica. Extremophiles 7(1), 55–61. doi: https://doi.org/10.1007/s00792-002-0295-2

    Article  PubMed  CAS  Google Scholar 

  2. de la Haba RR, Sánchez-Porro C, Márquez MC, Ventosa A (2011) Taxonomy of halophiles. In: Horikoshi K (ed) Extremophiles handbook. Springer, Heidelberg, pp 255–308. doi: https://doi.org/10.1007/978-4-431-53898-1_13

    Chapter  Google Scholar 

  3. Vreeland RH, Litchfield CD, Martin EL, Elliot E (1980) Halomonas elongata, a new genus and species of extremely salt-tolerant bacteria. Int J Syst Bacteriol 30:485–495

    Article  CAS  Google Scholar 

  4. Franzmann PD, Burton HR, McMeekin TA (1987) Halomonas subglaciescola, a new species of halotolerant bacteria isolated from Antarctica. Int J Syst Bacteriol 37:27–34

    Article  Google Scholar 

  5. Franzmann PD, Wehmeyer U, Stackebrandt E (1988) Halomonadaceae fam. nov., a new family of the class Proteobacteria to accommodate the genera Halomonas and Deleya. Syst Appl Microbiol 11:16–19

    Article  Google Scholar 

  6. Mormile MR, Romine MF, Garcia MT, Ventosa A, Bailey TJ, Peyton BM (1999) Halomonas campisalis sp. nov., a denitrifying, moderately haloalkaliphilic bacterium. Syst Appl Microbiol 22:551–558

    Article  CAS  PubMed  Google Scholar 

  7. Duckworth AW, Grant WD, Jones BE, Meijer D, Márquez MC. Ventosa A (2000) Halomonas magadii sp. nov., a new member of the genus Halomonas, isolated from a soda lake of the East African Rift Valley. Extremophiles 4(1): 53–60.

    Google Scholar 

  8. Oueriaghli N, González-Domenech C, Martínez-Checa F, Muyzer G, Ventosa A, Quesada A, Béjar V (2013) Diversity and distribution of Halomonas in Rambla Salada, a hypersaline environment in the southeast of Spain. FEMS Microbiol Ecol 87:460–474

    Article  CAS  PubMed  Google Scholar 

  9. Arahal DR, Vreeland RH, Litchfield CD, Mormile MR, Tindall BJ, Oren A, Bejar V, Quesada E, Ventosa A (2007) Recommended minimal standards for describing new taxa of the family Halomonadaceae. Int J Syst Evol Microbiol 57:2436–2446

    Article  CAS  PubMed  Google Scholar 

  10. Jadhav K, Kushwah B, Jadhav I (2018) Insight into compatible solutes from halophiles: exploring significant applications in biotechnology. In: Singh J., Sharma D., Kumar G., Sharma N. (eds) Microbial bioprospecting for sustainable development. Springer, Singapore.

    Google Scholar 

  11. Kushwah B, Jadhav I, Verma HN, Geethadevi A, Parashar D, Jadhav K (2019) Betaine accumulation suppresses the de-novo synthesis of ectoine at a low osmotic concentration in Halomonas sp SBS 10, a bacterium with broad salinity tolerance. Mol Biol Rep. https://doi.org/10.1007/s11033-019-04924-2

    Article  Google Scholar 

  12. Thomas T, Elain A, Bazire A, Stéphane Bruzaud (2019) Complete genome sequence of the halophilic PHA-producing bacterium Halomonas sp. SF2003: insights into its biotechnological potential. World J Microbiol Biotechnol 35(3): 50. doi: https://doi.org/10.1007/s11274-019-2627-8.

    Article  PubMed  CAS  Google Scholar 

  13. Stiller LM, Galinski EA, Witt E (2018) Engineering the salt-inducible Ectoine promoter region of Halomonas elongata for protein expression in a unique stabilizing environment. Genes 9(4):184. https://doi.org/10.3390/genes9040184

    Article  PubMed Central  CAS  Google Scholar 

  14. Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:272–328

    PubMed  CAS  Google Scholar 

  15. de la Haba RR, Arahal DR, Sánchez-Porro C, Ventosa A (2014) The family Halomonadaceae. Prokaryotes. https://doi.org/10.1007/978-3-642-38922-1_235

    Article  Google Scholar 

  16. Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  17. Embley TM (1991) The linear PCR reaction: a simple and robust method for sequencing amplified rRNA genes. Lett Appl Microbiol 13:171–174

    Article  CAS  PubMed  Google Scholar 

  18. Kumar S, Stecher G, Tamura K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. doi: https://doi.org/10.1093/molbev/msw054.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Arahal DR, Castillo AM, Ludwig W, Schleifer KH, Ventosa A (2002) Proposal of Cobetia marina gen. nov., comb. nov., within the family Halomonadaceae, to include the species Halomonas marina. Syst Appl Microbiol 25:207–211

    Article  PubMed  Google Scholar 

  20. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Method for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 607–654

    Google Scholar 

  21. Buck JD (1982) Nonstaining (KOH) method for determination of gram reactions of marine bacteria. Appl Environ Microbiol 44:992–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Mata JA, Martínez-Cánovas J, Quesada E, Béjar V (2002) A detailed phenotypic characterization of the type strains of Halomonas species. Syst Appl Microbiol 25:360–375

    Article  CAS  PubMed  Google Scholar 

  23. Cappuccino JG, Sherman N (2005) Microbiology: a laboratory manual, 7th edn. Benjamin Cummings, New York

    Google Scholar 

  24. Cowan ST, Steel KJ (1965) Manual for the identification of medical bacteria. Cambridge University Press, London

    Google Scholar 

  25. Ventosa A, Quesada E, Rodríguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1982) Numerical taxonomy of moderately halophilic Gram-negative rods. J Gen Microbiol 128:959–1968

    Google Scholar 

  26. Quesada E, Ventosa A, Ruiz-Berraquero F, Ramos-Cormenzana A (1984) Deleya halophila, a new species of moderately halophilic bacteria. Int J Syst Bacteriol 34:287–292

    Article  CAS  Google Scholar 

  27. Description of Kushneria aurantia gen. nov., sp. nov., a novel member of the family Halomonadaceae, and a proposal for reclassification of Halomonas marisflavi as Kushneria marisflavi comb. nov., of Halomonas indalinina as Kushneria indalinina comb. nov. and of Halomonas avicenniae as Kushneria avicenniae comb. nov. Int J Syst Evol Microbiol 59:397–405

    Article  CAS  PubMed  Google Scholar 

  28. Quesada E, Ventosa A, Ruiz-Berraquero F, Megias L, Ramos-Cormenzana A (1983) Numerical taxonomy of moderately halophilic gram-negative bacteria from hypersaline Soils. J General Microbiol 129:2649–2657

    Google Scholar 

  29. Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45(4):493–496

    Article  CAS  PubMed  Google Scholar 

  30. Bouchotroch S, Quesada E, Moral Ad, Llamas I, Bejar V (2001) Halomonas maura sp. nov., a novel moderately halophilic, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 51:1625–1632

    Article  CAS  PubMed  Google Scholar 

  31. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP, Zaslavsky L, Lomsadze A, Pruitt KD, Borodovsky M, Ostell J (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 44(14):6614–6624. https://doi.org/10.1093/nar/gkw569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. https://doi.org/10.1093/nar/gkt1226

    Article  PubMed  Google Scholar 

  33. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  34. de la Haba RR, Márquez MC, Papke RT, Ventosa A (2012) Multilocus sequence analysis of the familyHalomonadaceae. Int J Syt Evol Microbiol 62:520–538

    Article  CAS  Google Scholar 

  35. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol. 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  PubMed  PubMed Central  Google Scholar 

  37. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V, Fiebig A, Rohde C, Rohde M, Fartmann B, Goodwin LA, Chertkov O, Reddy T, Pati A, Ivanova NN, Markowitz V, Kyrpides NC, Woyke T, Göker M, Klenk HP (2014) Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 9:2. https://doi.org/10.1186/1944-3277-9-2

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rivera-Terceros P, Tito-Claros E, Torrico S, Carballo S, Van-Thuoc D, Quillaguamán J (2015) Production of poly(3-hydroxybutyrate) by Halomonas boliviensis in an air-lift reactor. J Biological Res 22(1):8. https://doi.org/10.1186/s40709-015-0031-6

    Article  CAS  Google Scholar 

  39. Kushwaha B, Sharma GP, Sharma A,Shankar P, Geethadevi A, Sharma N, Sharma MK, Jadhav I, Parashar D, Jadhav K (2020) Whole-genome shotgun sequence of Halomonas sp. strain SBS 10, isolated from a hypersaline lake in India. Microbiol Resour Announc 9:e01270-19. https://doi.org/10.1128/MRA.01270-19.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118

    Article  CAS  PubMed  Google Scholar 

  41. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    PubMed  CAS  Google Scholar 

  42. Pikuta EV, Itoh T, Krader P, Tang J, Whitman WB, Hoover B (2006) Anaerovirgula multivorans gen. nov., sp. nov., a novel spore-forming, alkaliphilic anaerobe isolated from Owens Lake. California. Int J Syst Evol Microbiol 53:2623–2629

    Article  CAS  Google Scholar 

  43. Qin QL et al (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196(12):2210–2215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wang YN, Cai H, Yu SL, Wang ZY, Liu J, Wu XL (2007) Halomonas gudaonensis sp. nov., isolated from a saline soil contaminated by crude oil. Int J Syst Evol Microbiol 57:911–915

    Article  CAS  PubMed  Google Scholar 

  45. Martínez-Cánovas MJ, Quesada E, Llamas I, Béjar V (2004) Halomonas ventosae sp. nov., a moderately halophilic, denitrifying, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 54:733–737

    Article  CAS  PubMed  Google Scholar 

  46. González-Domenech CM, Martínez-Checa F, Quesada E, Béjar V (2008) Halomonas cerina sp. nov., a moderately halophilic, denitrifying, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 58:803–809. https://doi.org/10.1099/ijs.0.65322-0

    Article  PubMed  CAS  Google Scholar 

  47. Luque R, Béjar V, Quesada E, Martínez-Checa F, Llamas I (2012) Halomonas ramblicola sp. nov., a moderately halophilic bacterium from Rambla Salada, Mediterranean hypersaline rambla. Int J Syst Evol Microbiol 62:2903–2909. https://doi.org/10.1099/ijs.0.039453-0

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Belgium Coordinated Collection of Microorganisms (BCCM), Gent, Belgium and CSIR-Institute of Microbial Technology, Chandigarh, India for providing the necessary facilities for deposition of culture in the general repository. The authors would also like to thank MNIT, Jaipur for Transmission Electron Microscopy.

Author information

Authors and Affiliations

  1. School of Life Sciences, Jaipur National University, Jaipur, India

    Bijayendra Kushwaha & Indrani Jadhav

  2. School of Engineering and Technology, Jaipur National University, Jaipur, India

    Kapilesh Jadhav

Authors
  1. Bijayendra Kushwaha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Indrani Jadhav
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kapilesh Jadhav
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BK conducted the experiments. IJ and KJ prepared the manuscript. All authors approved the manuscript and its submission.

Corresponding author

Correspondence to Kapilesh Jadhav.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The type strain, SBS 10T (= MTCC 12313T = LMG 30344T), and the strain SSO 06 (= MTCC 12312 = LMG 30343) were isolated from the saltern crystallizer ponds of the hypersaline Sambhar Salt Lake in India.

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequence of the strain SBS 10T is KT796562. The accession number for the draft genome sequences of the strain SBS 10T is RXHI00000000.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 122 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kushwaha, B., Jadhav, I. & Jadhav, K. Halomonas sambharensis sp. nov., a Moderately Halophilic Bacterium Isolated from the Saltern Crystallizer Ponds of the Sambhar Salt Lake in India. Curr Microbiol 77, 1125–1134 (2020). https://doi.org/10.1007/s00284-020-01892-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-020-01892-w

Search

Navigation