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Occurrence of Halococcus spp. in the nostrils salt glands of the seabird Calonectris diomedea

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Abstract

The nostrils of the seabird Calonectris diomedea are endowed with a salt-excreting gland that could produce a suitable environment for the colonization of extreme halophilic prokaryotes. We have studied in this organ the presence of extreme halophiles by means of culturing techniques. We could easily cultivate members of haloarchaea, and all cultures studied were identified as members of one of the two species Halococcus morrhuae and Hcc. dombrowskii. In order to reveal the diversity of these colonizers, we undertook a taxonomic study. Altogether, the results indicated that members of the genus Halococcus may constitute a part of the natural epizootic microbiota of C. diomedea, and that they exhibit such an important degree of taxonomic variability that appeals for a pragmatic species definition. This seabird nests in the west Mediterranean coasts, but its migratory habits, reaching locations as distant from the Mediterranean as the South Atlantic, may help in the dispersal mechanisms of haloarchaea through the Earth’s surface.

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References

  • Antón J, Rosselló-Móra R, Rodríguez-Valera F, Amann R (2000) Extremely halophilic bacteria in crystallizer ponds from solar salterns. Appl Environ Microbiol 66:3052–3057

    Article  PubMed  Google Scholar 

  • Benlloch S, Acinas SG, Antón J, López-López A, Luz SP, Rodríguez-Valera F (2001) Archaeal biodiversity in crystallizer ponds from a solar saltern: culture versus PCR. Microb Ecol 41:12–19

    PubMed  CAS  Google Scholar 

  • Christensen H, Bisgaard M, Frederiksen W, Mutters R, Kuhnert P, Olsen E (2001) Is characterization of a single isolate sufficient for valid publication of a new genus or species? Proposal to modify recommendation 30b of the Bacteriological Code (1990 revision). Int J Syst Evol Microbiol 51:2221–2225

    PubMed  CAS  Google Scholar 

  • Farlow WG (1880) On the nature of the peculiar reddening of salted codfish during the summer season. US Fish Comm Rep for 1878, pp 969–973

  • Figuerola J, Green AJ, Michot TC (2005) Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. Am Nat 165:274–278

    Article  PubMed  Google Scholar 

  • Goh F, Leuko S, Allen MA, Bowman JP, Kamekura M, Neilan BA, Burns BP (2006) Halococcus hamelinensis sp. nov., a novel halophilic archaeon isolated from stromatolites in Shark Bay, Australia. Int J Syst Evol Microbiol 56:1323–1329

    Article  PubMed  CAS  Google Scholar 

  • González-Solís J, Croxall JP, Oro D, Ruiz X (2007) Transequatorial migration and mixing in the wintering area in a pelagic seabird. Front Ecol Environ 5:297–301

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Javor BJ (1984) Growth potential of halophilic bacteria isolated from solar salt environments: carbon sources and salt requirements. Appl Environ Microbiol 48:352–360

    PubMed  CAS  Google Scholar 

  • Javor BJ (1989) Hypersaline environments. Microbiology and Biogeochemistry. Brock/Springer series in contemporary bioscience. Springer, Berlin

    Google Scholar 

  • Kellogg CA, Griffin DW (2006) Aerobiology and the global transport of desert dust. Trends Ecol Evol 21:638–644

    Article  PubMed  Google Scholar 

  • Kocur M, Hodgkiss W (1973) Taxonomic status of the genus Halococcus Schoop. Int J Syst Bacteriol 23:151–156

    Article  Google Scholar 

  • Konstantinidis K, Tiejde JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509

    Article  PubMed  CAS  Google Scholar 

  • Larsen H (1989) Genus IV Halococcus. In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 3. Williams & Wilkins, Baltimore, pp 2228–2230

    Google Scholar 

  • Leuko S, Goh F, Ibáñez-Peral R, Burns BP, Walter MR, Neilan BA (2007) Lysis efficiency of standard DNA extraction methods for Halococcus spp. in an organic rich environment. Extremophiles 12:301–308

    Article  PubMed  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar Buchner A, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  • Maturrano L, Santos F, Rosselló-Móra R, Antón J (2006) Microbial diversity in Maras salterns, a hypersaline environment in the Peruvian Andes. Appl Environ Microbiol 72:3887–3895

    Article  PubMed  CAS  Google Scholar 

  • Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–172

    Article  PubMed  CAS  Google Scholar 

  • Namwong S, Tanasupawat S, Visessanguan W, Kudo T, Itoh T (2007) Halococcus thailandensis sp. nov., from fish sauce in Thailand. Int J Syst Evol Microbiol 57:2199–2203

    Article  PubMed  CAS  Google Scholar 

  • Oren A (1994) The ecology of the extremely halophilic Archaea. FEMS Microbiol Rev 13:415–440

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pedrós-Alió C (2005) Diversity of microbial communities: the case of solar salterns. In: Gunde-Cimerman, Oren A, Plemenitas A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria and Eucarya. Springer, Dordrecht (The Netherlands), pp 71–90

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  PubMed  CAS  Google Scholar 

  • Purdy KJ, Cresswell-Maynard TD, Nedwell DB, McGenity TJ, Grant WD, Timmis KN, Embley TM (2004) Isolation of haloarchaea that grow at low salinities. Environ Microbiol 6:591–595

    Article  PubMed  CAS  Google Scholar 

  • Rainey FA, Ray K, Ferreira M, Gatz BZ, Nobre MF, Bagaley D, Rash BA, Park MJ, Earl AM, Shank NC, Small AM, Henk MC, Battista JR, Kämpfer P, Da Costa MS (2005) Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran desert soil, and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl Environ Microbiol 71:5225–5235

    Article  PubMed  CAS  Google Scholar 

  • Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240

    PubMed  CAS  Google Scholar 

  • Rodríguez-Valera F, Ruiz-Berraquero F, Ramos-Cormenzana A (1979) Isolation of extreme halophiles from seawater. Appl Environ Microbiol 38:164–165

    PubMed  Google Scholar 

  • Rosselló-Móra R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  Google Scholar 

  • Rosselló-Móra R, Lucio M, Peña A, Brito-Echeverría J, López-López A, Valens-Vadell M, Frommberger M, Antón J, Schmitt-Kopplin P (2008) Metabolic evidence for biogeographic isolation of the extremophilic bacterium Salinibacter ruber. ISME J 2:242–253

    Article  PubMed  CAS  Google Scholar 

  • Smibert RM, Krieg RN (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Manual of methods for general microbiology. American Society for Microbiology, Washington DC, pp 607–654

    Google Scholar 

  • Sória-Carrasco V, Valens-Vadell M, Peña A, Antón J, Amann R, Castresana R, Rosselló-Móra R (2007) Phylogenetic position of Salinibacter ruber based on concatenated protein alignments. Syst Appl Microbiol 30:171–179

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Stackebrandt E, Frederiksen W, Garrity G, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Rosselló-Móra R, Swings J, Trüper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047

    Article  PubMed  CAS  Google Scholar 

  • Stahl DA, Amann RI (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Sequencing and hybridization techniques in bacterial systematics. Wiley, Chichester, pp 205–248

    Google Scholar 

  • Stan-Lotter H, Pfaffenhuemer M, Legat A, Busse HJ, Radax C, Gruber C (2002) Halococcus dombrowskii sp. nov., an archaeal isolate from a Permian alpine salt deposit. Int J Syst Evol Microbiol 52:1807–1814

    Article  PubMed  CAS  Google Scholar 

  • Urdiain M, López-López A, Gonzalo C, Busse HJ, Langer S, Kämpfer P, Rosselló-Móra R (2008) Reclassification of Rhodobium marinum and Rhodobium pfennigii as Afifella marina gen. nov. comb. nov. and Afifella pfennigii comb. nov., a new genus of photoheterotrophic Alphaproteobacteria and emended descriptions of Rhodobium, Rhodobium orientis and Rhodobium gokarnense. Syst Appl Microbiol 31:339–351

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Li W, Yang H, Liu Y, Cao H, Dornmayr-Pfaffenhuemer M, Stan-Lotter H, Guo G (2007) Halococcus qingdaonensis sp. nov., a halophilic archaeon isolated from a crude sea-salt sample. Int J Syst Evol Microbiol 57:600–604

    Article  PubMed  CAS  Google Scholar 

  • Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464

    Google Scholar 

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Acknowledgements

The authors want to acknowledge the help in the sampling strategy given by the Population Ecology Group of the IMEDEA and especially Daniel Oro for his collaboration. The project has been funded by the projects CLG2006-12714-C02-01 and CLG2006-12714-C02-02 of the Spanish Ministerio de Ciencia e Innovación.

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Correspondence to Jocelyn Brito-Echeverría.

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Communicated by F. Robb.

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Brito-Echeverría, J., López-López, A., Yarza, P. et al. Occurrence of Halococcus spp. in the nostrils salt glands of the seabird Calonectris diomedea . Extremophiles 13, 557–565 (2009). https://doi.org/10.1007/s00792-009-0238-2

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