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Ecophysiological diversity of a novel member of the genus Alteromonas, and description of Alteromonas mediterranea sp. nov.

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Abstract

Nine non-pigmented, motile, Gram-negative bacteria originally designated as Alteromonas macleodii deep-sea ecotypes, were isolated from seawater samples collected from four separate locations; two deep-sea sites in the Mediterranean Sea and surface water of the Aegean Sea and English Channel. The six strains studied in vitro were found to tolerate up to 20 % NaCl. The DNA–DNA relatedness between the deep-sea ecotype strains was found to be between 75 and 89 %, whilst relatedness with the validly named Alteromonas species was found to be between 31 and 69 %. The average nucleotide identity (ANI) amongst the deep-sea ecotype strains was found to be 98–100 %; the in silico genome-to-genome distance (GGD), 85–100 %; the average amino acid identity (AAI) of all conserved protein-coding genes, 95–100 %; and the strains possessed 30–32 of the Karlin’s genomic signature dissimilarity. The ANI between the deep-sea ecotype strains and A. macleodii ATCC 27126T and Alteromonas australica H 17T was found to be 80.6 and 74.6 %, respectively. A significant correlation was observed between the phenotypic data obtained in vitro and data retrieved in silico from whole genome sequences. The results of a phylogenetic study that incorporated a 16S rRNA gene sequence analysis, multilocus phylogenetic analysis (MLPA) and genomic analysis, together with the physiological, biochemical and chemotaxonomic data, clearly indicated that the group of deep-sea ecotype strains represents a distinct species within the genus Alteromonas. Based on these data, a new species, Alteromonas mediterranea, is proposed. The type strain is DET ( = CIP 110805T = LMG 28347T = DSM 17117T).

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Amaral GRS, Dias GM, Wellington-Oguri M, Chimetto L, Campeão ME, Thompson FL, Thompson CC (2014) Genotype to phenotype: identification of diagnostic vibrio phenotypes using whole genome sequences. Int J Syst Evol Microbiol 64:357–365

    Article  CAS  PubMed  Google Scholar 

  • Azegami K, Nishiyama K, Watanabe Y, Kadota I, Ohuchi A, Fukazawa C (1987) Pseudomonas plantarii sp. nov., the causal agent of rice seeding blight. Int J Syst Evol Microbiol 37:144–152

    Google Scholar 

  • Baumann P, Baumann L (1981) The marine Gram-negative eubacteria; genera Photobacterium, Beneckea, Alteromonas, Pseudomonas, and Alcaligenes. In: Starr MP, Starr MP, Stolp HG, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes a handbook on habitats, isolation, and identification of bacteria. Springer-Verlag, Berlin, pp 1302–1330

    Google Scholar 

  • Baumann P, Baumann L, Mandel M, Allen RD (1972) Taxonomy of aerobic marine eubacteria. J Bacteriol 110:402–429

    CAS  PubMed Central  PubMed  Google Scholar 

  • Baumann P, Gauthier MJ, Baumann L (1984) Genus Alteromonas. Baumann, Baumann, Mandel and Allen 1972. In: Krieg NR, Holt JG (eds) Bergey`s Manual of Systematic Bacteriology. Williams & Wilkins Co, Baltimore, pp 243–354

    Google Scholar 

  • Chen YG, Xiao HD, Tang SK, Zhang YQ, Borrathybay E, Cui XL, Li WJ, Liu YQ (2009) Alteromonas halophila sp. nov., a new moderately halophilic bacterium isolated from a sea anemone. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 96:259–266

    Article  CAS  Google Scholar 

  • Chiu HH, Shieh WY, Lin SY, Tseng CM, Chiang PW, Wagner-Döbler I (2007) Alteromonas tagae sp. nov. and Alteromonas simiduii sp. nov., mercury-resistant bacteria isolated from a Taiwanese estuary. Int J Syst Evol Microbiol 57:1209–1216

    Article  CAS  PubMed  Google Scholar 

  • Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Didelot X, Lawson D, Darling A, Falush D (2010) Inference of homologous recombination in bacteria using whole-genome sequences. Genetics 186:1435–1449

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • García-Martínez J, Acinas SG, Massana R, Rodríguez-Valera F (2002) Prevalence and microdiversity of Alteromonas macleodii-like microorganisms in different oceanic regions. Environ Microbiol 4:42–50

    Article  PubMed  Google Scholar 

  • Gauthier G, Gauthier M, Christen R (1995) Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int J Syst Evol Microbiol 45:755–761

    CAS  Google Scholar 

  • Gonzalez JM, Saiz-Jimenez C (2005) A simple fluorimetric method for the estimation of DNA-DNA relatedness between closely related microorganisms by thermal denaturation temperatures. Extremophiles 9:75–79

    Article  CAS  PubMed  Google Scholar 

  • Goris J, Suzuki KI, De Vos P, Nakase T, Kersters K (1998) Evaluation of a microplate DNA–DNA hybridization method compared with the initial renaturation method. Can J Microbiol 44:1148–1153

    Article  CAS  Google Scholar 

  • Hagström Å, Pinhassi J, Zweifel UL (2000) Biogeographical diversity among marine bacterioplankton. Aquatic Microb Ecol 21:231–244

    Article  Google Scholar 

  • Ivanova EP, Flavier S, Christen R (2004) Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov. and Psychromonadaceae fam. nov. Int J Syst Evol Microbiol 54:1773–1788

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Bowman JP, Lysenko AM, Zhukova NV, Gorshkova NM, Kuznetsova TA, Kalinovskaya NL, Shevchenko LS, Mikhailov VV (2005a) Erythrobacter vulgaris sp. nov., a novel organism isolated from the marine invertebrates. Syst Appl Microbiol 28:123–130

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Bowman JP, Lysenko AM, Zhukova NV, Gorshkova NM, Sergeev AF, Mikhailov VV (2005b) Alteromonas addita sp. nov. Int J Syst Evol Microbiol 55:1065–1068

    Article  CAS  PubMed  Google Scholar 

  • Ivanova EP, Ng HJ, Webb HK, Kurilenko VV, Zhukova NV, Mikhailov VV, Ponamoreva ON, Crawford RJ (2013) Alteromonas australica sp. nov., isolated from the Tasman Sea. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 103:877–884

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ivars-Martínez E, Martin-Cuadrado AB, D’Auria G, Mira A, Ferriera S, Johnson J, Friedman R, Rodriguez-Valera F (2008b) Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter. ISME J 2:1194–1212

    Article  PubMed  Google Scholar 

  • Karlin S, Mrazek J, Campbell AM (1997) Compositional biases of bacterial genomes and evolutionary implications. J Bacteriol 179:3899–3913

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • López-López A, Bartual SG, Stal L, Onyshchenko O, Rodríguez-Valera F (2005) Genetic analysis of housekeeping genes reveals a deep-sea ecotype of Alteromonas macleodii in the Mediterranean Sea. Environ Microbiol 7:649–659

    Article  PubMed  Google Scholar 

  • López-Pérez M, Gonzaga A, Martin-Cuadrado AB, Onyshchenko O, Ghavidel A, Ghai R, Rodriguez-Valera F (2012) Genomes of surface isolates of Alteromonas macleodii: the life of a widespread marine opportunistic copiotroph. Sci Rep 2:696

    Article  PubMed Central  PubMed  Google Scholar 

  • López-Pérez M, Gonzaga A, Rodriguez-Valera F (2013) Genomic diversity of “deep ecotype” Alteromonas macleodii isolates: evidence for pan-mediterranean clonal frames. Genome Biol Evol 5:1220–1232

    Article  PubMed Central  PubMed  Google Scholar 

  • López-Pérez M, Gonzaga A, Ivanova EP, Rodriguez-Valera F (2014) Genomes of Alteromonas australica, a world apart. BMC Genomics 15:483

    Article  PubMed Central  PubMed  Google Scholar 

  • Martínez-Checa F, Béjar V, Llamas I, del Moral A, Quesada E (2005) Alteromonas hispanica sp. nov., a polyunsaturated-fatty-acid-producing, halophilic bacterium isolated from Fuente de Piedra, southern Spain. Int J Syst Evol Microbiol 55:2385–2390

    Article  PubMed  Google Scholar 

  • Ng HJ, Webb HK, Crawford RJ, Malherbe F, Butt H, Knight R, Mikhailov VV, Ivanova EP (2013) Updating the taxonomic toolbox: classification of Alteromonas spp. using multilocus phylogenetic analysis and MALDI-TOF mass spectrometry. Antonie van Leeuwenhoek Int J Gen Mol Microbiol 103:877–884

    Article  Google Scholar 

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sass AM, Sass H, Coolen MJL, Cypionka H, Overmann J (2001) Microbial communities in the chemocline of a hypersaline Deep-Sea Basin (Urania Basin, Mediterranean Sea). Appl Environ Microbiol 67:5392–5402

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Landschoot A, De Ley J (1983) Intra- and intergeneric similarities of the rRNA cistrons of Alteromonas, Marinomonas (gen. nov.) and some other gram-negative bacteria. J Gen Micorbiol 129:3057–3074

    Google Scholar 

  • Van Trappen S, Tan TL, Yang J, Mergaert J, Swings J (2004) Alteromonas stellipolaris sp. nov., a novel, budding, prosthecate bacterium from Antarctic seas, and emended description of the genus Alteromonas. Int J Syst Evol Microbiol 54:1157–1163

    Article  PubMed  Google Scholar 

  • Vandecandelaere I, Nercessian O, Segaert E, Achouak W, Mollica A, Faimali M, De Vos P, Vandamme P (2008) Alteromonas genovensis sp. nov., isolated from a marine electroactive biofilm and emended description of Alteromonas macleodii Baumann et al. 1972 (Approved Lists 1980). Int J Syst Evol Microbiol 58:2589–2596

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Yoon JH, Yeo SH, Oh TK, Park YH (2004) Alteromonas litorea sp. nov., a sllightly halophilic bacterium isolated from an intertidal sediment of the Yellow Sea in Korea. Int J Syst Evol Microbiol 54:1197–1201

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was partially supported by funds from Australian Research Council (ARC). The authors would like to thank Jun Ng for performing the MALDI-TOF MS analysis and Bio21 Institute for access to the MALDI-TOF MS instrument.

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Correspondence to Elena P. Ivanova.

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Ivanova, E.P., López-Pérez, M., Zabalos, M. et al. Ecophysiological diversity of a novel member of the genus Alteromonas, and description of Alteromonas mediterranea sp. nov.. Antonie van Leeuwenhoek 107, 119–132 (2015). https://doi.org/10.1007/s10482-014-0309-y

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