Skip to main content
Log in

Diversity of actinomycetes isolated from Challenger Deep sediment (10,898 m) from the Mariana Trench

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

Abstract

Thirty-eight actinomycetes were isolated from sediment collected from the Mariana Trench (10,898 m) using marine agar and media selective for actinomycetes, notably raffinose-histidine agar. The isolates were assigned to the class Actinobacteria using primers specific for members of this taxon. The phylogenetic analysis based on 16S rRNA gene sequencing showed that the isolates belonged to the genera Dermacoccus, Kocuria, Micromonospora, Streptomyces, Tsukamurella and Williamsia. All of the isolates were screened for genes encoding nonribosomal peptide and polyketide synthetases. Nonribosomal peptide synthetase sequences were detected in more than half of the isolates and polyketide synthases type I (PKS-I) were identified in five out of 38 strains. The Streptomyces isolates produced several unusual secondary metabolites, including a PKS-I associated product. In initial testing for piezotolerance, the Dermacoccus strain MT1.1 grew at elevated hydrostatic pressures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Akimoto K, Hattori M, Uematsu K, Kato C (2001) The deepest living foraminifera, Challenger Deep, Mariana Trench. Mar Micropaleontol 42:95–97

    Article  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  PubMed  Google Scholar 

  • Attwell RW, Colwell RR (1984) Thermoactinomycetes as terrestrial indicators for marine and estuarine waters. In: Ortiz-Ortiz L, Bojalil LF, Yakoleff V (eds) Biological, biochemical and biomedical aspects of actinomycetes. Academic Press, Orlando, pp 441–452

    Google Scholar 

  • Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24

    Article  PubMed  Google Scholar 

  • Brandão FFB, Bull AT (2003) Nitrile hydrolyzing activities of deep-sea and terrestrial mycolate actinomycetes. Antonie van Leeuwenhoek 84:89–98

    Article  PubMed  Google Scholar 

  • Brandão PFB, Clapp JP, Bull AT (2002) Discrimination and taxonomy of geographically diverse strains of nitrile-metabolizing actinomycetes using chemometric and molecular sequencing techniques. Environ Microbiol 4:262–276

    Article  PubMed  Google Scholar 

  • Bull AT (2004) Bountiful oceans: prospecting marine microbial diversity. Screen Trends Drug Discov 5:14–16

    Google Scholar 

  • Bull AT, Goodfellow M, Slater JH (1992) Biodiversity as a source of innovation in biotechnology. Annu Rev Microbiol 42:219–257

    Article  Google Scholar 

  • Bull AT, Stach JEM, Ward AC, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges and future directions. Antonie van Leeuwenhoek 87:65–79

    Article  Google Scholar 

  • Colquhoun JA, Mexson J, Goodfellow M, Ward AC, Horikoshi K, Bull AT (1998) Novel rhodococci and other mycolate actinomycetes from the deep sea. Antonie van Leeuwenhoek 74:27–40

    Article  PubMed  Google Scholar 

  • Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, Martinez A, Kolvek SJ, Hopke J, Osburne MS, August PR, Nalin R, Guerineau M, Jeannin P, Simonet P, Pernodet JL (2003) Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 69:49–55

    Article  PubMed  Google Scholar 

  • Cross T (1968) Thermophilic actinomycetes. J Appl Bacteriol 31:36–53

    PubMed  Google Scholar 

  • Duangmal K, Ward AC, Goodfellow M (2005) Selective isolation of members of the Streptomyces violaceoruber clade from soil. FEMS Microbiol Lett 245:321–327

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogeny: an appropriate use of the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Fiedler H-P, Bruntner C, Bull AT, Ward AC, Goodfellow M, Mihm G (2005) Marine actinomycetes as a source of novel secondary metabolites. Antonie van Leeuwenhoek 87:37–42

    Article  PubMed  Google Scholar 

  • Finking R, Marahiel AM (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 28:453–488

    Article  Google Scholar 

  • Ginolhac A, Jarrin C, Gillet B, Robe P, Pujic P, Tuphile K, Bertrand H, Vogel TM, Perriere G, Simonet P, Nalin R (2004) Phylogenetic analysis of polyketide synthase I domains from soil metagenomic libraries allows selection of promising clones. Appl Environ Microbiol 70:5522–5527

    Article  PubMed  Google Scholar 

  • Goodfellow M, Haynes JA (1984) Actinomycetes in marine sediments. In: Ortiz–Ortiz L, Bojalil LF, Yakoleff V (eds) Biological, biochemical and biomedical aspects of actinomycetes. Academic Press, Orlando, pp 453–472

    Google Scholar 

  • Gvirtzman Z, Stern RJ (2004) Bathymetry of Mariana trench-arc system and formation of the Challenger Deep as a consequence of weak plate coupling. Tectonics 23(Art no. TC2011)

  • Han SK, Nedashkovskaya OI, Mikhailov V, Kim SB, Bae KS (2003) Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int J Syst Evol Microbiol 53:2061–2066

    Article  PubMed  Google Scholar 

  • Hayakawa M, Nonomura H (1987) Humic acid vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65:501–509

    Article  Google Scholar 

  • Heald SC, Brandão PFB, Hardicre R, Bull AT (2001) Physiology, biochemistry and taxonomy of deep-sea nitrile metabolising Rhodococcus strains. Antonie van Leeuwenhoek 80:169–183

    Article  PubMed  Google Scholar 

  • Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M (2002) Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol 68:2391–2396

    Article  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, et al (1998) Multiple sequence alignment with CLUSTAL X. Trends Biochem Sci 23(10):403–405

    Article  PubMed  Google Scholar 

  • Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments. Appl Environ Microbiol 57:1102–1108

    PubMed  Google Scholar 

  • Jensen PR, Mincer TJ, Williams PG, Fenical W (2005) Marine actinomycete diversity and natural product discovery. Antonie van Leeuwenhoek 87:43–48

    Article  PubMed  Google Scholar 

  • Joseph SJ, Hugenholtz P, Sangwan P, Osbone CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69:7210–7215

    Article  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, N Y, pp 21–132

  • Kato C, Li L, Nogi Y, Nakamura Y, Tamaoka J, Horikoshi K (1998) Extremely barophilic bacteria isolated from the Mariana Trench, Challenger Deep, at a depth of 11,000 meters. Appl Environ Microbiol 64:1510–1513

    PubMed  Google Scholar 

  • Kato C, Li L, Tamaoka J, Horikoshi K (1997) Molecular analyses of the sediment of the 11,000-m-deep of the Mariana Trench. Extremophiles 1:117–123

    Google Scholar 

  • Kelly KL (1958) Centroid notations for the revised ISCC-NBS color name blocks. J Res Nat Bureau Standards USA 61:472

    Google Scholar 

  • Ketela MM, Virpi S, Halo L, Hautala A, Hakala J, Mantsala P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6

    PubMed  Google Scholar 

  • Ketela MM, Halo L, Manukka E, Hakala J, Mantsala P, Ylihonko K (2002) Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various Streptomyces species. Appl Environ Microbiol 68:4472–4479

    Article  PubMed  Google Scholar 

  • Kim SB, Falconer C, Williams E, Goodfellow M (1998) Streptomyces thermocarboxydovorans sp. nov. and Streptomyces thermocarboxydus sp. nov., two moderately thermophilic carboxydotrophic species from soil. Int J Syst Bacteriol 48:59–68

    PubMed  Google Scholar 

  • Kyo M, Miyazaki E, Tsukioka S, Ochi H, Amitani Y, Tsuchiya T, Aoki T, Takagawa S (1995) The sea trial of “KAIKO”, the full ocean depth research ROV. Oceans 95:1991–1996

    Google Scholar 

  • Lanoot B, Vancanneyt M, Dawyndt P, Cnockaert M, Zhang J, Huang Y, Liu Z, Swings J (2004) BOX-PCR fingerprinting as a powerful tool to reveal synonymous names in the genus Streptomyces. Emended descriptions are proposed for the species Streptomyces cinereorectus, S. fradiae, S. tricolor, S. colombiensis, S. filamentosus, S. vinaceus and S. phaeopurpureus. Syst Appl Microbiol 27:84–92

    Article  PubMed  Google Scholar 

  • Liu W, Ahlert J, Gao Q, Pienkowski EW, Shen B, Thorson JS (2003) Rapid PCR amplification of minimal enediyne polyketide synthase cassettes leads to a predictive familial classification model. Proc Natl Acad Sci 100:11959–11963

    Article  PubMed  Google Scholar 

  • Maldonado LA, Stach JEM, Pathom-aree W, Ward AC, Bull AT, Goodfellow M (2005) Diversity of cultivable actinobacteria in geographically widespread marine sediments. Antonie van Leeuwenhoek 87:11–18

    Article  PubMed  Google Scholar 

  • Mincer TJ, Jensen PR, Kauffmann CA, Fenical W (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 68:5005–5011

    Article  PubMed  Google Scholar 

  • National Bureau of Standards (1964) ISCC-NBS color-name charts illustrated with centroid colors (supplement to national bureau of standards USA circular 553). National Bureau of Standards, USA

  • Olive DM, Bean P (1999) Principles and applications of methods for DNA-based typing of microbial organisms. J Clin Microbiol 37:1661–1669

    PubMed  Google Scholar 

  • Pearson K (1926) On the coefficient of racial likeness. Biometrika 18:105–117

    Google Scholar 

  • Sadowsky MJ, Kinnel LL, Bowers JH, Schottel JL (1996) Use of repetitive intergenic DNA sequences to classify pathogenic and disease-suppressive Streptomyces strains. Appl Environ Microbiol 62:3489–3493

    PubMed  Google Scholar 

  • Sait M, Hugenholtz P, Janssen PH (2002) Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4:654–666

    Article  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

    PubMed  Google Scholar 

  • Schaal KP (1977) Nocardia, Actinomadura and Streptomyces. In: CRC handbook series in clinical laboratory science, section E, clinical microbiology. CRC Press, Cleveland, OH, pp 131–158

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Google Scholar 

  • Stach JEM, Maldonado LA, Ward AC, Goodfellow M, Bull AT (2003a) Statistical approaches to estimating bacterial diversity in marine sediments. Appl Environ Microbiol 69:6189–6200

    Article  PubMed  Google Scholar 

  • Stach JEM, Maldonado LA, Ward AC, Goodfellow M, Bull AT (2003b) New primers for the class Actinobacteria: application to marine and terrestrial environments. Environ Microbiol 5:828–841

    Article  PubMed  Google Scholar 

  • Taira K, Kitagawa S, Yamashiro T, Yanagimoto D (2004) Deep and bottom currents in the Challenger Deep, Mariana trench, measured with super-deep current meters. J Oceanogr 60:919–926

    Article  Google Scholar 

  • Takami H, Inoue A, Fuji F, Horikoshi K (1997) Microbial flora in the deepest sea mud of the Mariana Trench. FEMS Microbiol Lett 152:279–285

    PubMed  Google Scholar 

  • Takizawa M, Colwell ER, Hill RT (1993) Isolation and diversity of actinomycetes in Chesapeake Bay. Appl Environ Microbiol 59:997–1002

    PubMed  Google Scholar 

  • Van der Peer Y, de Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Versalovic J, Schneider M, de Bruijn FJ, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25–40

    Google Scholar 

  • Vickers JC, Williams ST, Ross GW (1984) A taxonomic approach to selective isolation of streptomycetes from soil. In: Ortiz–Ortiz L, Bojalil LF, Yakoleff V (eds) Biological, biochemical and biomedical aspects of actinomycetes. Academic Press, Orlando, pp 553–561

  • Ward JH (1963) Hierarchical grouping to optimise an objective function. J Am Statist Assoc 58:236–244

    Google Scholar 

  • Weyland H (1981) Distribution of actinomycetes on the sea floor. Actinomycetes. Zbl Bakt 11(Suppl):185–193

    Google Scholar 

  • Yamamura H, Hayakawa M, Nakagawa Y, Iimura Y (2004) Characterization of Nocardia asteroides isolates from different ecological habitats on the basis of repetitive extragenic palindromic-PCR fingerprinting. Appl Environ Microbiol 70:3149–3151

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Kaiko operation team and the crew of M.S. Yokosuka for collecting sediment samples and Professor David Manning (School of Civil Engineering and Geomatics, University of Newcastle) for the use of the pressure equipment. Wasu Pathom-aree is also grateful to the Royal Thai Government and to the DPST program for financial support. ATB, MG and ACW also gratefully acknowledge support from the UK Natural Environmental Research Council (grants NER/T/S/2000/00614 and NER/T/S/ 2000/00616). We thank two anonymous reviewers for their constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wasu Pathom-aree.

Additional information

Communicated by A. Driessen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pathom-aree, W., Stach, J.E.M., Ward, A.C. et al. Diversity of actinomycetes isolated from Challenger Deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10, 181–189 (2006). https://doi.org/10.1007/s00792-005-0482-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-005-0482-z

Keywords

Navigation