Skip to main content
SpringerLink
Log in

Taxonomy of halophilic Archaea: current status and future challenges

  • Special Issue: Review
  • 10th International Congress on Extremophiles
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Several groups of Archaea, all Euryarchaeota, develop in hypersaline environments (from >10 % salt up to saturation). The cultured diversity of halophilic Archaea includes the family Halobacteriaceae of aerobic or facultative anaerobic, generally red-pigmented species (47 genera and 165 species as of February 2014) and seven representatives of four genera of methanogens, most of which obtain energy from methylated amines under anaerobic conditions. Metagenomic studies have identified an additional deep lineage of Archaea in salt lakes and ponds with brines approaching NaCl saturation. Genomic information is now available for representatives of these ‘Nanohaloarchaea’, but no members of this lineage have yet been cultured. Multilocus sequence analysis is becoming increasingly popular in taxonomic studies of the Halobacteriaceae, and such studies have demonstrated that recombination of genetic traits occurs at an extremely high frequency at least in some genera. Metagenomic studies in an Antarctic lake showed that large identical regions of up to 35 kb in length can be shared by members of different genera living together in the same environment. Such observations have important implications not only for the taxonomy of the Halobacteriaceae, but also for species concepts and questions on taxonomy and classification for prokaryotic microorganisms in general.

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

ANI:

Average nucleotide identity

MLSA:

Multilocus sequence analysis

Hbt. :

Halobacterum

Hfx. :

Haloferax

Hht. :

Halohasta

Hqr. :

Haloquadratum

Hrr. :

Halorubrum

References

  • Amann G, Stetter KO, Llobet-Brossa E, Amann R, Antón J (2000) Direct proof for the presence and expression of two 5% different 16S rRNA genes in individual cells of Haloarcula marismortui. Extremophiles 4:373–376

    Article  CAS  PubMed  Google Scholar 

  • Andrei A-Ş, Banciu HL, Oren A (2012) Metabolic diversity in Archaea living in saline ecosystems. FEMS Microbiol Lett 330:1–9

    Article  CAS  PubMed  Google Scholar 

  • Arahal DR, Oren A, Ventosa A (2011) International Committee on Systematics of Prokaryotes. Subcommittee on the taxonomy of Halobacteriaceae and Subcommittee on the taxonomy of Halomonadaceae. Minutes of the joint open meeting, 6 September 2011, Sapporo, Japan. Int J Syst Evol Microbiol 61:2792–2795

    Article  Google Scholar 

  • Bolhuis H, te Poele EM, Rodríguez-Valera F (2004) Isolation and cultivation of Walsby’s square archaeon. Environ Microbiol 6:1287–1291

    Article  PubMed  Google Scholar 

  • Bolhuis H, Palm P, Wende A, Falb M, Rampp M, Rodriguez-Valera F, Pfeiffer F, Oesterhelt D (2006) The genome of the square archaeon Haloquadratum walsbyi: life at the limits of water activity. BMC Genom 7:169

    Article  Google Scholar 

  • Boone DR (2001) Genus IV. Methanohalophilus Paterek and Smith 1988, 122VP. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. The Archaea and the deeply branching and phototrophic Bacteria. Springer, New York, pp 281–283

  • Boone DR, Baker CC (2001) Genus VI. Methanosalsum gen. nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. The Archaea and the deeply branching and phototrophic Bacteria. Springer, New York, pp 287–289

  • Boone DR, Mathrani IM, Liu Y, Menaia JAGF, Mah RA, Boone JE (1993) Isolation and characterization of Methanohalophilus portucalensis sp. nov. and DNA reassociation study of the genus Methanohalophilus. Int J Syst Bacteriol 43:430–437

    Article  Google Scholar 

  • Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004a) Cultivation of Walsby’s square haloarchaeon. FEMS Microbiol Lett 238:469–473

    CAS  PubMed  Google Scholar 

  • Burns DG, Camakaris HM, Janssen PH, Dyall-Smith ML (2004b) Combined use of cultivation-dependent and cultivation-independent methods indicates that members of most haloarchaeal groups in an Australian crystallizer pond are cultivable. Appl Environ Microbiol 70:5258–5265

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Burns DG, Janssen PH, Itoh T, Kamekura M, Li Z, Jensen G, Rodríguez-Valera F, Bolhuis H, Dyall-Smith ML (2007) Haloquadratum walsbyi gen. nov., sp. nov., the square haloarchaeon of Walsby, isolated from saltern crystallizers in Australia and Spain. Int J Syst Evol Microbiol 57:387–392

    Article  CAS  PubMed  Google Scholar 

  • Casanueva A, Galada N, Baker GC, Grant WD, Heaphy S, Jones B, Yanhe M, Ventosa A, Blamey J, Cowan DA (2008) Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments. Extremophiles 12:651–656

    Article  CAS  PubMed  Google Scholar 

  • Chimileski S, Dolas K, Naor A, Gophna U, Papke RT (2014) Extracellular DNA metabolism in Haloferax volcanii. Frontiers Microbiol 5:57

    Google Scholar 

  • Cui H-L, Zhou P-J, Oren A, Liu S-J (2009) Intraspecific polymorphism of 16S rRNA genes in two halophilic archaeal genera, Haloarcula and Halomicrobium. Extremophiles 13:31–37

    Article  CAS  PubMed  Google Scholar 

  • Davidova IA, Harmsen HJM, Stams AJM, Belyaev SS, Zehnder AJB (1997) Taxonomic description of Methanococcoides euhalobius and its transfer to the Methanohalophilus genus. Antonie van Leeuwenhoek 71:313–318

    Article  CAS  PubMed  Google Scholar 

  • DeMaere MZ, Williams TJ, Allen MA, Brown MV, Gibson JAE, Rich J, Lauro FM, Dyall-Smith M, Davenport KW, Woyke T, Kyrpides NC, Tringe SG, Cavicchioli R (2013) High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc Natl Acad Sci 110:16939–16944

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dennis PP, Ziesche S, Mylvaganam S (1998) Transcription analysis of two disparate rRNA operons in the halophilic archaeon Haloarcula marismortui. J Bacteriol 180:4804–4813

    CAS  PubMed Central  PubMed  Google Scholar 

  • Di Meglio L, Busalamen J, Pastore JI, Ballarin D, Nercessian D (2014) Hyperhalophilic archaeal biofilms: growth kinetics, structure, and antagonistic interaction in continuous culture. Biofouling 30:237–245

    Article  PubMed  Google Scholar 

  • Franzmann PD, Stackebrandt E, Sanderson K, Volkman JK, Cameron DE, Stevenson PL, McMeekin TA, Burton HR (1988) Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica. Syst Appl Microbiol 11:20–27

    Article  CAS  Google Scholar 

  • Fröls S, Dyall-Smith M, Pfeifer F (2012) Biofilm formation by haloarchaea. Environ Microbiol 14:3159–3174

    Article  PubMed  Google Scholar 

  • Ghai R, Fernández AB, Martin-Cuadrado A-B, Megumi Mizuno C, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, Sánchez-Porro C, Ventosa A, Rodríguez-Valera F (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1:135

    Article  PubMed Central  PubMed  Google Scholar 

  • Gibson JAE, Miller MR, Davies NW, Neill P, Nichols DS, Volkmann JK (2005) Unsaturated diether lipids in the psychrotrophic archaeon Halorubrum lacusprofundi. Syst Evol Microbiol 28:19–26

    Article  CAS  Google Scholar 

  • Grant S, Grant WD, Jones BE, Kato C, Li L (1999) Noval archaeal phylotypes from an East African alkaline saltern. Extremophiles 3:139–145

    Article  CAS  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005) Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci 102:2567–2572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kushner DJ (1978) Life in high salt and solute concentrations: halophilic bacteria. In: Kushner DJ (ed) Microbial life in extreme environments. Academic Press, London, pp 317–368

    Google Scholar 

  • Legault BA, Lopez-Lopez A, Alba-Casado JC, Doolittle WF, Bolhuis H, Rodríguez-Valera F, Papke RT (2006) Environmental genomics of “Haloquadratum walsbyi” in a saltern crystallizer indicates a large pool of accessory genes in an otherwise coherent species. BMC Genom 7:171

    Article  Google Scholar 

  • Liu Y, Boone DR, Choy C (1990) Methanohalophilus oregonense sp. nov., a methylotrophic methanogen from an alkaline, saline aquifer. Int J Syst Bacteriol 40:111–116

    Article  Google Scholar 

  • López-López A, Benlloch S, Bonfá M, Rodríguez-Valera F, Mira A (2007) Intragenomic 16S DNA divergence in Haloarcula marismortui is an adaptation to different temperatures. J Mol Evol 65:687–969

    Article  PubMed  Google Scholar 

  • Magrum LJ, Luehrsen KR, Woese CR (1978) Are extreme halophiles actually “bacteria”? J Mol Evol 11:1–8

    Article  CAS  PubMed  Google Scholar 

  • Mathrani IM, Boone DR, Mah RA, Fox GE, Lau PP (1988) Methanohalophilus zhilinae sp. nov., an alkaliphilic, halophilic, methylotrophic methanogen. Int J Syst Bacteriol 38:139–142

    Article  CAS  PubMed  Google Scholar 

  • McGenity TJ (2010) Methanogens and methanogenesis in hypersaline environments. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer-Verlag, Berlin, pp 665–680

    Chapter  Google Scholar 

  • Mevarech M, Hirsch-Twizer S, Goldman S, Yakobson E, Eisenberg H, Dennis PP (1989) Isolation and characterization of the rRNA gene clusters of Halobacterium marismortui. J Bacteriol 171:3479–3485

    CAS  PubMed Central  PubMed  Google Scholar 

  • Minegishi H, Kamekura M, Itoh T, Echigo A, Usami R, Hashimoto T (2010) Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B’ (rpoB′ ) gene. Int J Syst Evol Microbiol 60:2398–2408

    Article  PubMed  Google Scholar 

  • Minegishi H, Kamekura M, Kitajima-Ihara T, Nakasone K, Echigo A, Shimane Y, Usami R, Itoh T, Ihara K (2012) Gene orders in the upstream of 16S rRNA genes divide genera of the family Halobacteriaceae into two groups. Int J Syst Evol Microbiol 62:188–195

    Article  CAS  PubMed  Google Scholar 

  • Mou Y-Z, Qiu X–X, Zhao M-L, Cui H-L, Oh D, Dyall-Smith ML (2012) Halohasta litorea gen. nov., and Halohasta litchfieldiae sp. nov., isolated from the Daliang aquaculture farm, China and from Deep Lake, Antarctica, respectively. Extremophiles 16:895–901

    Article  CAS  PubMed  Google Scholar 

  • Naor A, Lapierre P, Mevarech M, Papke RT, Gophna U (2012) Low species barriers in halophilic archaea and the formation of recombinant hybrids. Curr Biol 22:1444–1448

    Article  CAS  PubMed  Google Scholar 

  • Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelberg KB, Banfield JF, Allen EE (2012) De novo assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 6:81–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInterney JO, Deppenmeier U, Martin WF (2012) Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci 109:20537–20542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oh D, Porter K, Russ B, Burns D, Dyall-Smith M (2010) Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds. Extremophiles 14:161–169

    Article  PubMed Central  PubMed  Google Scholar 

  • Ollivier B, Fardeau M-L, Cayol J-L, Magot M, Patel BKC, Prensier G, Garcia J-L (1998) Methanocalculus halotolerans gen. nov., sp. nov., isolated from an oil-producing well. Int J Syst Bacteriol 48:821–828

    Article  PubMed  Google Scholar 

  • Oren A (2012) Taxonomy of the family Halobacteriaceae: a paradigm for changing concepts in prokaryote systematics. Int J Syst Evol Microbiol 62:263–271

    Article  PubMed  Google Scholar 

  • Oren A (2014a) Family Methanosarcinaceae. In: Rosenberg E, DeLong EF, Thompson F, Lory S, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, 4th edn. Springer, New York

    Google Scholar 

  • Oren A (2014b) Family Methanocalculaceae. In: Rosenberg E, DeLong EF, Thompson F, Lory S, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, 4th edn. Springer, New York

    Google Scholar 

  • Oren A (2014c) Family Halobacteriaceae. In: Rosenberg E, DeLong EF, Thompson F, Lory S, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, 4th edn. Springer, New York

    Google Scholar 

  • Oren A, Garrity GM (2014) Then and now: a systematic review of the systematics of prokaryotes in the last 80 years. Antonie van Leeuwenhoek. doi:10.1007/s10482-013-0084-1

    PubMed  Google Scholar 

  • Oren A, Ventosa A (2008) International Committee on Systematics of Prokaryotes. Subcommittee on the taxonomy of Halobacteriaceae. Minutes of the meetings, 7 August 2008, Istanbul, Turkey. Int J Syst Evol Microbiol 58:2465–2467

    Article  Google Scholar 

  • Oren A, Ventosa A (2010) International Committee on Systematics of Prokaryotes. Subcommittee on the taxonomy of Halobacteriaceae and Subcommittee on the taxonomy of Halomonadaceae. Minutes of the meeting 30 June 2010, Beijing, China. Int J Syst Evol Microbiol 60:2257–2259

    Article  Google Scholar 

  • Oren A, Ventosa A (2013) International Committee on Systematics of Prokaryotes. Subcommittee on the taxonomy of Halobacteriaceae and Subcommittee on the taxonomy of Halomonadaceae. Minutes of the joint open meeting, 24 June 2013, Storrs, Connecticut, USA. Int J Syst Evol Microbiol 63:3540–3544

    Article  PubMed Central  PubMed  Google Scholar 

  • Oren A, Ventosa A, Grant WD (1997) Proposal of minimal standards for the description of new taxa in the order Halobacteriales. Int J Syst Bacteriol 47:233–238

    Article  Google Scholar 

  • Oren A, Vreeland RH, Ventosa A (2007) International Committee on Systematics of Prokaryotes. Subcommittee on the taxonomy of Halobacteriaceae and Subcommittee on the taxonomy of Halomonadaceae. Minutes of the joint open meeting, 3 September 2007, Colchester, UK. Int J Syst Evol Microbiol 57:2975–2978

    Article  Google Scholar 

  • Oren A, Arahal DR, Ventosa A (2009) Emended descriptions of genera of the family Halobacteriaceae. Int J Syst Evol Microbiol 59:637–642

    Article  PubMed  Google Scholar 

  • Papke RT, Gogarten JP (2012) How bacterial lineages emerge. Science 336:45–46

    Article  PubMed  Google Scholar 

  • Papke RT, Koenig JE, Rodríguez-Valera F, Doolittle WF (2004) Frequent recombination in a saltern population of Halorubrum. Science 306:1928–1929

    CAS  PubMed  Google Scholar 

  • Papke RT, Zhaxybayeva O, Feil EJ, Sommerfeld K, Muise D, Doolittle WF (2007) Searching for species in haloarchaea. Proc Natl Acad Sci 104:14092–14097

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Papke RT, White E, Reddy P, Weigel G, Kamekura M, Minegishi H, Usami R, Ventosa A (2011) A multilocus sequence analysis approach to the phylogeny and taxonomy of the Halobacteriales. Int J Syst Evol Microbiol 61:2984–2995

    Article  CAS  PubMed  Google Scholar 

  • Paterek JR, Smith PH (1988) Methanohalophilus mahii gen. nov., sp. nov., a methylotrophic halophilic methanogen. Int J Syst Bacteriol 38:122–123

    Article  Google Scholar 

  • Rosenshine I, Tchelet R, Mevarech M (1989) The mechanism of DNA transfer in the mating system of an archaebacterium. Science 245:1387–1389

    Article  CAS  PubMed  Google Scholar 

  • Soppa J (2013) Evolutionary advantages of polyploidy in halophilic archaea. Biochem Soc Trans 41:339–343

    Article  CAS  PubMed  Google Scholar 

  • Spring S, Scheuner C, Lapidus A, Lucas S, Glavina Del Rio T, Tice H, Copeland A, Cheng JF, Chen F, Nolan M, Saunders E, Pitluck S, Liolios K, Ivanova N, Mavromatis K, Lykidis A, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Goodwin L, Detter JC, Brettin T, Rohde M, Göker M, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2010) The genome sequence of Methanohalophilus mahii SLPT reveals differences in the energy metabolism among members of the Methanosarcinaceae inhabiting freshwater and saline environments. Archaea 2010:690737

    Article  PubMed Central  PubMed  Google Scholar 

  • Trüper HG (2005) Is ‘localimania’ becoming a fashion for prokaryote taxonomists? Int J Syst Evol Microbiol 45:1753

    Article  Google Scholar 

  • Vreeland RH, Straight S, Krammes J, Dougherty K, Rosenzweig WD, Kamekura M (2002) Halosimplex carlsbadense gen. nov., sp. nov., a unique halophilic archaeon, with three 16S rRNA genes, that grows only in defined medium with glycerol and acetate or pyruvate. Extremophiles 6:445–452

    Article  CAS  PubMed  Google Scholar 

  • Walsby AE (1980) A square bacterium. Nature 283:69–71

    Article  Google Scholar 

  • Wilharm T, Zhilina TN, Hummel P (1991) DNA–DNA hybridization of methylotrophic halophilic methanogenic bacteria and transfer of Methanococcus halophilus VP to the genus Methanohalophilus as Methanohalophilus halophilus comb. nov. Int J Syst Bacteriol 41:558–562

    Article  Google Scholar 

  • Yu IK, Kawamura F (1987) Halomethanococcus doii gen. nov., sp. nov.: an obligately halophilic methanogenic bacterium from solar salt ponds. J Gen Appl Microbiol 33:303–310

    Article  CAS  Google Scholar 

  • Zhilina TN (1983) A new obligate halophilic methane-producing bacterium. Mikrobiologiya 52:375–382

    CAS  Google Scholar 

  • Zhilina TN (2001) Genus III. Methanohalobium Zhilina and Zavarzin 1988, 136VP (Effective publication: Zhilina and Zavarzin 1987a, 467). In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 1, 2nd edn. The Archaea and the deeply branching and phototrophic Bacteria. Springer, New York, pp 279–281

  • Zhilina TN, Zavarzin GA (1987) Methanohalobium evestigatus n. gen., n. sp. The extremely halophilic methanogenic Archaebacterium. Dokl Akad Nauk SSSR 293:464–468 (in Russian)

    CAS  Google Scholar 

  • Zhilina TN, Zavarzina DG, Kevbrin VV, Kolganova TV (2013) Methanocalculus natronophilus sp. nov., a new alkaliphilic hydrogenotrophic methanogenic archaeon from a soda lake, and proposal of the new family Methanocalculaceae. Microbiology (Russ) 82:686–694

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant and Environmental Sciences, The Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel

    Aharon Oren

Authors
  1. Aharon Oren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aharon Oren.

Additional information

Communicated by G. Antranikian.

This article is part of a special issue based on the 10th International Congress on Extremophiles held in Saint Petersburg, Russia, September 7–11, 2014.

Three-letter abbreviations for genera of Halobacteriaceae were used as recommended (Oren and Ventosa 2013)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oren, A. Taxonomy of halophilic Archaea: current status and future challenges. Extremophiles 18, 825–834 (2014). https://doi.org/10.1007/s00792-014-0654-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-014-0654-9

Keywords

Search

Navigation