Skip to main content
SpringerLink
Log in

Acid-shifted isoelectric point profiles of the proteins in a hypersaline microbial mat: an adaptation to life at high salt concentrations?

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

In a metagenomic analysis of a stratified hypersaline (9 % salt) microbial mat in Guerrero Negro, Mexico, Kunin et al. (Mol Systems Biol 4:198, 2008) detected a significantly acid-shifted proteome, and concluded that adaptation by enriching proteins with acidic amino acids is more widespread than previously assumed. We here reevaluate these data and conclusions by comparing the isoelectric point profiles of the Guerrero Negro microbial mats (average isoelectric point 6.8) with those of the proteins encoded by the genomes of prokaryotes adapted to different salt concentrations ranges and belonging to different phylogenetic and physiological groups. Average isoelectric points below 6.8 were found not only in the proteomes of the moderately halophilic aerobic bacteria Halomonas elongata and Chromohalobacter salexigens, but even in common types of marine bacteria of the genera Alteromonas and Aliivibrio. We did not find clear evidence that the isoelectric point profile of the Guerrero Negro microbial mat can be considered to be the result of species-independent molecular convergence of the members of the microbial community determined by the salinity of the overlaying brine.

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
Fig. 4

Similar content being viewed by others

References

  • Antón J, Oren A, Benlloch S, Rodríguez-Valera F, Amann R, Rosselló-Mora R (2002) Salinibacter ruber gen. nov., sp. nov., a novel extreme halophilic member of the bacteria from saltern crystallizer ponds. Int J Syst Evol Microbiol 52:485–491

    PubMed  Google Scholar 

  • Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J (2010) Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol, Chap 19, Unit 19.10.1–21

  • Elevi Bardavid R, Oren A (2012) The amino acid composition of proteins from anaerobic halophilic bacteria of the order Halanaerobiales. Extremophiles 16:567–572

    Article  PubMed  CAS  Google Scholar 

  • Fiala G, Woese CR, Langworthy TA, Stetter KO (1990) Flexistipes sinusarabici, a novel genus and species of eubacteria occurring in the Atlantis II Deep brines of the Red Sea. Arch Microbiol 154:120–126

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ghai R, Martin-Cuadrado AB, Gonzaga Molto A, García Heredia I, Cabrera R, Martin J, Verdú M, Deschamps P, Moreira D, López-García P, Mira A, Rodriguez-Valera F (2010) Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing. ISME J 4:1154–1166

    Article  PubMed  CAS  Google Scholar 

  • Ghai R, Pašić L, Fernández AB, Martin-Cuadrado A-B, Megumi Mizuno C, McMahon KD, Papke RT, Stepanauskas R, Rodríguez-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  Google Scholar 

  • Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, Miller W, Kent WJ, Nekrutenko A (2005) Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15:1451–1455

    Article  PubMed  CAS  Google Scholar 

  • Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappé MS, Short JM, Carrington JC, Mathur EJ (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245

    Article  PubMed  CAS  Google Scholar 

  • Goecks J, Nekrutenko A, Taylor J, The Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86

    Article  PubMed  Google Scholar 

  • Ivanova N, Sikorski J, Chertkov O, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng J-F, Tapia R, Han C, Goodwin L, Pitluck S, Huntemann M, Liolios K, Pagani I, Mavromatis K, Ovchinnikova G, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Brambilla E-M, Palani Kannan K, Rohde M, Tindall BJ, Göker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk H-P, Lapidus A (2011) Complete genome sequence of the extremely halophilic Halanaerobium praevalens type strain (GSLT). Stand Genomic Sci 4:312–321

    Article  PubMed  CAS  Google Scholar 

  • Ivars-Martínez E, D’Auria G, Rodríguez-Valera F, Sánchez-Porro C, Ventosa A, Ioint I, Mühling M (2008) Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis. Mol Ecol 17:4092–4106

    Article  PubMed  Google Scholar 

  • Kunin V, Raes J, Harris JK, Spear JR, Walker JJ, Ivanova N, von Mering C, Bebout BM, Pace NR, Bork P, Hugenholtz P (2008) Millimeter-scale genetic gradients and community-level molecular convergence in a hypersaline microbial mat. Mol Syst Biol 4:198

    Article  PubMed  Google Scholar 

  • Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 38:272–290

    PubMed  CAS  Google Scholar 

  • Lapidus A, Chertkov O, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng J-F, Tapia R, Han C, Goodwin L, Pitluck S, Liolios K, Pagani I, Ivanova N, Huntemann M, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Brambilla E-M, Rohde M, Abt B, Spring S, Göker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk H-P, Woyke T (2011) Genome sequence of the moderately thermophilic halophile Flexistipes sinusarabici strain (MAS10T). Stand Genomic Sci 5:86–96

    Article  PubMed  CAS  Google Scholar 

  • Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature 458:215–218

    Article  PubMed  CAS  Google Scholar 

  • Mesbah NM, Hedrick DB, Peacock AD, Rohde M, Wiegel J (2007) Natranaerobius thermophilus gen. nov., sp. nov., a halophilic, alkalithermophilic bacterium from soda lakes of the Wadi An Natrun, Egypt, and proposal of Natranaerobiaceae fam. nov. and Natranaerobiales ord. nov. Int J Syst Evol Microbiol 57:2507–2512

    Article  PubMed  CAS  Google Scholar 

  • Mevarech M, Frolow F, Gloss LM (2000) Halophilic enzymes: proteins with a grain of salt. Biophys Chem 86:155–164

    Article  PubMed  CAS  Google Scholar 

  • Mongodin EF, Nelson KE, Daugherty S, DeBoy RT, Wister J, Khouri H, Weidman J, Walsh DA, Papke RT, Sanchez-Perez G, Sharma AK, Nesbø CL, MacLeod D, Bapteste E, Doolittle WF, Charlebois RL, Legault B, Rodriguez-Valera F (2005) The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc Natl Acad Sci USA 102:18147–18152

    Article  PubMed  CAS  Google Scholar 

  • Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga NS, Thorsson V, Sbrogna J, Swartzell S, Weir D, Hall J, Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP, Angevine CM, Dale H, Isenbarger TA, Peck RF, Pohlschroder M, Spudich JL, Jung K-H, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omer AD, Ebhardt H, Lowe TM, Liang P, Riley M, Hood L, DasSarma S (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci USA 97:12176–12181

    Article  PubMed  CAS  Google Scholar 

  • Oren A (2006) Life at high salt concentrations. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. A handbook on the biology of bacteria: ecophysiology and biochemistry, vol 2. Springer, New York, pp 263–282

    Google Scholar 

  • Oren A, Larimer F, Richardson P, Lapidus A, Csonka LN (2005) How to be moderately halophilic with a broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles 9:275–279

    Article  PubMed  CAS  Google Scholar 

  • Reistad R (1970) On the composition and nature of the bulk protein of extremely halophilic bacteria. Arch Mikrobiol 71:353–360

    Article  PubMed  CAS  Google Scholar 

  • Rhodes ME, Fitz-Gibbon S, Oren A, House CH (2010) Amino acid signatures of salinity on an environmental scale with a focus on the Dead Sea. Environ Microbiol 12:2613–2623

    Article  PubMed  CAS  Google Scholar 

  • Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers Y-H, Falcón LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77

    Article  PubMed  Google Scholar 

  • Schwibbert K, Marin-Sanguino A, Bagyan I, Heidrich G, Lentzen G, Seitz H, Rampp M, Schuster SC, Klenk H-P, Pfeiffer F, Oesterhelt D, Kunte HJ (2011) A blueprint of ectoine metabolism from the genome of the industrial producer Halomonas DSM 2581. Environ Microbiol 13:1973–1994

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Mesbah NM, Dalin E, Goodwin L, Nolan M, Pitluck S, Chertkov O, Brettin TS, Han J, Larimer FW, Land ML, Hauser L, Kyrpides N, Wiegel J (2011) Complete genome sequence of the anaerobic, halophilic alkalithermophilic Natranaerobius thermophilus. J Bacteriol 193:4023–4024

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grant no. 1103/10 from the Israel Science Foundation.

Author information

Authors and Affiliations

  1. Department of Plant and Environmental Sciences, The Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel

    Rahel Elevi Bardavid & Aharon Oren

Authors
  1. Rahel Elevi Bardavid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. 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 M. da Costa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elevi Bardavid, R., Oren, A. Acid-shifted isoelectric point profiles of the proteins in a hypersaline microbial mat: an adaptation to life at high salt concentrations?. Extremophiles 16, 787–792 (2012). https://doi.org/10.1007/s00792-012-0476-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-012-0476-6

Keywords

Search

Navigation