Skip to main content
SpringerLink
Log in

Halomonas tabrizica sp. nov., a novel moderately halophilic bacterium isolated from Urmia Lake in Iran

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

A novel moderately halophilic, Gram-stain negative and aerobic bacterium, designated strain TBZ21T, was isolated from a water sample of Urmia Lake, Iran. Cells were observed to be non-motile rods with no flagellum, showing positive catalase and oxidase reactions. Strain TBZ21T was found to grow at 10–40 °C (optimum, 30 °C), at pH 7–10 (optimum, pH 8) and in the presence of 1–22% (optimum, 10%). The major fatty acids were identified as C19:0 cyclo ω8c, C16:0, Summed features 3 (C13:0 3-OH and/or iso-C15:1 H) and 8 (C18:1 ω7c and/or C18:1 ω6c) and C12:0 3-OH. The major polar lipids were identified as diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and an unidentified phosphoaminolipid. The genomic DNA G+C content of strain TBZ21T was determined to be 63.3 mol%. Phylogenetic analyses based on 16S rRNA gene sequences indicated that strain TBZ21T belongs to the genus Halomonas, and shows high sequence similarities to Halomonas fontilapidosi 5CRT (99.43%), Halomonas ventosae AL12T (98.64%), Halomonas sediminicola CPS11T (98.63%) and Halomonas aestuarii Hb3T (98.08%), and has low similarities (below 98.0%) with other members of the genus. The values of DNA–DNA relatedness between strain TBZ21T and the closely related strains H. fontilapidosi LMG 24455T and H. ventosae LMG 26187T were 42 ± 11% and 54 ± 16%, respectively. On the basis of phenotypic, chemotaxonomic and molecular characteristics, strain TBZ21T is concluded to represent a novel species of the genus Halomonas, for which the name Halomonas tabrizica sp. nov. is proposed. The type strain is TBZ21T (=LMG 25445T=DSM 23018T).

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

Similar content being viewed by others

Abbreviations

KCCM:

Korean Culture Center of Microorganisms, Seoul, Republic of Korea

LMG LMG:

Culture collection, Universiteit Gent, Gent, Belgium

DDH DNA:

DNA hybridization

References

  • Alipour S (2006) Hydrogeochemistry of seasonal variation of Urmia salt Lake Iran. Saline Syst 2:1–9

    Article  CAS  Google Scholar 

  • Anan’ina LN, Plotnikova EG, Gavrish EIu, Demakov VA, Evtushenko LI (2007) Salinicola socius gen. nov., sp. nov., a moderately halophilic bacterium from a naphthalene-utilizing microbial association. Microbiology 76:369–376

    Article  PubMed  Google Scholar 

  • 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 

  • 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  PubMed  CAS  Google Scholar 

  • Ben Ali Gam Z, Abdelkafi S, Casalot L, Tholozan JL, Oueslati R, Labat M et al (2007) Modicisalibacter tunisiensis gen. nov., sp. nov., an aerobic, moderately halophilic bacterium isolated from an oilfield-water injection sample, and emended description of the family Halomonadaceae Franzmann, 1989 emend Dobson and Franzmann 1996 emend. Ntougias et al. 2007. Int J Syst Evol Microbiol 57:2307–2313

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cashion P, Holder-Franklin MA, McCully J, Franklin M (1977) A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 81:461–466

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dobson SJ, Franzmann PD et al (1996) Unification of the genera Deleya (Baumann,1983), Halomonas (Vreeland et al. 1980), and Halovibrio (Fendrich 1988) and the species Paracoccus halodenitrificans (Robinson & Gibbons 1952) into a single genus, Halomonas, and placement of the genus Zymobacter in the family Halomonadaceae. Int J Syst Evol Microbiol 46:550–558

    CAS  Google Scholar 

  • Eimanifar A, Mohebbi F (2007) Urmia Lake (Northwest Iran): a brief review. Saline Syst 3:1–5

    Article  Google Scholar 

  • Ezaki T, Hashimoto Y, Yabuuchi E (1989) Fluorometric deoxyribonucleic acid- deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39:224–229

    Article  Google Scholar 

  • Felsenstein J (2002) PHYLIP (phylogeny inference package), version 3.6a. University of Washington, Seattle

    Google Scholar 

  • Fendrich C (1988) Halovibrio variabilis gen. nov. sp. nov., Pseudomonas halophila sp. nov. and a new halophilic aerobic coccoid Eubacterium from Great Salt Lake, Utah USA. Syst Appl Microbiol 11:36–43

    Article  CAS  Google Scholar 

  • 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 

  • Garriga M, Ehrmann MA, Arnau J, Hugas M, Vogel RF (1998) Carnimonas nigrificans gen. nov., sp. nov., a bacterial causative agent for black spot formation on cured meat products. Int J Syst Evol Microbiol 48:677–686

    CAS  Google Scholar 

  • González-Domenech CM, Martínez-Checa F, Quesada E, Béjar V (2009) Halomonas fontilapidosi sp. nov., a moderately halophilic, denitrifying bacterium. Int J Syst Evol Microbiol 59:1290–1296

    Article  PubMed  CAS  Google Scholar 

  • Gregersen T (1978) Rapid method for distinction of prot-negative from Gram-positive bacteria. Appl Microbiol Biotechnol 5:123–127

    Article  Google Scholar 

  • Jeon CO, Lim JM, Lee JR, Lee GS, Park DJ, Lee JC, Oh HW, Kim CJ (2007) Halomonas kribbensis sp. nov., a novel moderately halophilic bacterium isolated from a solar saltern in Korea. Int J Syst Evol Microbiol 57:2194–2198

    Article  PubMed  CAS  Google Scholar 

  • Jung WY, Lee HJ, Jeon CO (2016) Halomonas garicola sp. nov., isolated from saeu-jeot, a Korean salted and fermented shrimp sauce. Int J Syst Evol Microbiol 66:731–737

    Article  PubMed  CAS  Google Scholar 

  • Kharroub K, Jiménez-Pranteda ML, Aguilera M, Boulahrouf A, Ramos-Cormenzana A, Monteoliva-Sánchez M (2008) Halomonas sabkhae sp. nov., a moderately halophilic bacterium isolated from an Algerian sabkha. Int J Syst Evol Microbiol 58:40–44

    Article  PubMed  CAS  Google Scholar 

  • Kim M, Oh HS, Park SC, Chun JS (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351

    Article  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular Evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lányí B (1987) Classical and rapid identification methods for medically important bacteria. Methods Microbiol 19:1–67

    Google Scholar 

  • León MJ, Sánchez-Porro C, de la Haba RR, Llamas I, Ventosa A (2014) Larsenia salina gen. nov., sp. nov., a new member of the family Halomonadaceae based on multilocus sequence analysis. Syst Appl Microbiol 37:480–487

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 Evol Microbiol 39:159–167

    CAS  Google Scholar 

  • Minnikin DE, Patel PV, Alshamaony L, Goodfellow M (1977) Polar lipid composition in the classification of Nocardia and related bacteria. Int J Syst Bacteriol 27:104–117

    Article  CAS  Google Scholar 

  • Nawrocki EP, Eddy SR (2007) Query-dependent banding (QDB) for faster RNA similarity searches. PLoS Comput Biol 3:e56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ntougias S, Zervakis GI, Fasseas C et al (2007) Halotalea alkalilenta gen. nov. sp. nov., a novel osmotolerant and alkalitolerant bacterium from alkaline olive mill wastes, and emended description of the family Halomonadaceae Franzmann, 1989, emend. Dobson and Franzmann 1996. Int J Syst Evol Microbiol 57:1975–1983

    Article  PubMed  CAS  Google Scholar 

  • Okamoto T, Taguchi H, Nakamura K, Ikenaga H, Kuraishi H, Yamasato K (1993) Zymobacter palmae gen. nov., sp. nov., a new ethanol-fermenting peritrichous bacterium isolated from palm sap. Arch Microbiol 160:333–337

    Article  PubMed  CAS  Google Scholar 

  • Romano I, Nicolaus B, Lama L, Manca MC, Gambacorta A (1996) Characterization of a haloalkalophilic strickly aerobic bacterium, isolated from Pantelleria Island. Syst Appl Microbiol 19:326–333

    Article  Google Scholar 

  • Rosselló-Móra R, Amann R (2015) Past and future species definitions for bacteria and archaea. Syst Appl Microbiol 38:209–216

    Article  PubMed  Google Scholar 

  • Rosselló-Móra R, Trujillo ME, Sutcliffe IC (2017) Introducing a digital protologue: a timely move towards a database-driven systematics of archaea and bacteria. Antonie Van Leeuwenhoek 110:455–456

    Article  PubMed  Google Scholar 

  • Sánchez-Porro C, Martin S, Mellado E, Ventosa A (2003) Diversity of moderately halophilic bacteria producing extracellular hydrolytic enzymes. J Appl Microbiol 94:295–300

    Article  PubMed  Google Scholar 

  • Sánchez-Porro C, de la Haba RR, Soto-Ramírez N, Márquez MC, Montalvo-Rodríguez R, Ventosa A (2009) 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  PubMed  CAS  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. MIDI Inc, Newark

    Google Scholar 

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

    Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 9:1312–1313

    Article  CAS  Google Scholar 

  • Tamaoka J, Komagata K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25:125–128

    Article  CAS  Google Scholar 

  • Vahed SZ, Forouhandeh H, Hassanzadeh S, Klenk HP, Hejazi MA, Hejazi MS (2011) Isolation and characterization of halophilic bacteria from Urmia Lake in Iran. Microbiology 80:826–833

    Article  PubMed  CAS  Google Scholar 

  • Ventosa A, Gutiérrez MC, García MT, Ruiz-Berraquero F (1989) Classification of “Chromobacterium marismortui” in a new genus, Chromohalobacter gen. nov., as Chromohalobacter marismortui comb. nov., nom. rev. Int J Syst Bacteriol 39:382–386

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

    Article  Google Scholar 

  • Vreeland RH, Martin EL (1980) Growth characteristics, effects of temperature, and ion specificity of the halotolerant bacterium Halomonas elongata. Can J Microbiol 26:746–752

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Wang YN, Cai H, Chi CQ, Lu AH, Lin XG, Jiang ZF, Wu XL (2007) Halomonas shengliensis sp. nov., a moderately halophilic, denitrifying, crude-oil-utilizing bacterium. Int J Syst Evol Microbiol 57:1222–1226

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Tang SK, Lou K, Lee JC, Jeon CO, Xu LH, Kim CJ, Li WJ (2009) Aidingimonas halophila gen. nov., sp. nov., a moderately halophilic bacterium isolated from a salt lake. Int J Syst Evol Microbiol 59:3088–3094

    Article  PubMed  CAS  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandle O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE et al (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol MicroBacteriol 37:463–464

    Article  Google Scholar 

  • Yoon JH, Lee KC, Kho YH, Kang KH, Kim CJ, Park YH (2002) Halomonas alimentaria sp. nov., isolated from jeotgal, a traditional Korean fermented seafood. Int J Syst Evol Microbiol 52:123–130

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  PubMed Central  Google Scholar 

  • Zepeda VK, Busse HJ, Golke J, Saw JH, Alam M, Donachie SP (2015) Terasakiispira papahanaumokuakeensis gen. nov., sp. nov., a gammaproteobacterium from pearl and hermes atoll, Northwestern Hawaiian Islands. Int J Syst Evol Microbiol 65:3609–3617

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to M. Akbari Dibavar and Poladi for their kind assistance.

Funding

This work was supported by the National Research Foundation (2017M3C1B5019250) of Ministry of Science and ICT, Republic of Korea. Tabriz University of Medical Sciences, Iran.

Author information

Author notes

  1. Sepideh Zununi Vahed, Haleh Forouhandeh and Yunho Lee have contributed equally to this work and should be considered as co-first authors.

Authors and Affiliations

  1. Department of Pharmaceutical Biotechnology, Faculty of Pharmacy, Tabriz University of Medical Sciences, Tabriz, Iran

    Sepideh Zununi Vahed, Vahideh Tarhriz & Mohammad Saeid Hejazi

  2. Kidney Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

    Sepideh Zununi Vahed

  3. Molecular Medicine Research Center, Biomedicine Institute, Tabriz University of Medical Sciences, Tabriz, Iran

    Haleh Forouhandeh, Vahideh Tarhriz & Mohammad Saeid Hejazi

  4. Department of Life Science, Chung-Ang University, 84, HeukSeok-Ro, Dongjak-Gu, Seoul, 06974, Republic of Korea

    Che Ok Jeon & Yunho Lee

  5. Department of Biology, Azarbaijan Shahid Madani University, Tabriz, Iran

    Nader Chaparzadeh

  6. Department of Food Biotechnology, Branch for Northwest & West Region, Agricultural Biotechnology Research Institute of Iran, Agricultural Research, Education and Extension Organization (AREEO), Tabriz, Iran

    Mohammad Amin Hejazi

Authors
  1. Sepideh Zununi Vahed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Haleh Forouhandeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vahideh Tarhriz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nader Chaparzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Amin Hejazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Che Ok Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mohammad Saeid Hejazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yunho Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Che Ok Jeon or Mohammad Saeid Hejazi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants and/or animals performed by any of the authors. The formal consent is not required in this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 599 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vahed, S.Z., Forouhandeh, H., Tarhriz, V. et al. Halomonas tabrizica sp. nov., a novel moderately halophilic bacterium isolated from Urmia Lake in Iran. Antonie van Leeuwenhoek 111, 1139–1148 (2018). https://doi.org/10.1007/s10482-018-1018-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-018-1018-8

Keywords

Search

Navigation