Diversity and Biosynthetic Potential of Culturable Actinomycetes Associated with Marine Sponges in the China Seas

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2012 Jul 4

PMID 22754340

Citations 16

Authors

Lijun Xi

Jisheng Ruan

Ying Huang

Affiliations

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Abstract

The diversity and secondary metabolite potential of culturable actinomycetes associated with eight different marine sponges collected from the South China Sea and the Yellow sea were investigated. A total of 327 strains were isolated and 108 representative isolates were selected for phylogenetic analysis. Ten families and 13 genera of Actinomycetales were detected, among which five genera represent first records isolated from marine sponges. Oligotrophic medium M5 (water agar) proved to be efficient for selective isolation, and "Micromonospora-Streptomyces" was proposed as the major distribution group of sponge-associated actinomycetes from the China Seas. Ten isolates are likely to represent novel species. Sponge Hymeniacidon perleve was found to contain the highest genus diversity (seven genera) of actinomycetes. Housekeeping gene phylogenetic analyses of the isolates indicated one ubiquitous Micromonospora species, one unique Streptomyces species and one unique Verrucosispora phylogroup. Of the isolates, 27.5% displayed antimicrobial activity, and 91% contained polyketide synthase and/or nonribosomal peptide synthetase genes, indicating that these isolates had a high potential to produce secondary metabolites. The isolates from sponge Axinella sp. contained the highest presence of both antimicrobial activity and NRPS genes, while those from isolation medium DNBA showed the highest presence of antimicrobial activity and PKS I genes.

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References

Mincer T, Fenical W, Jensen P . Culture-dependent and culture-independent diversity within the obligate marine actinomycete genus Salinispora. Appl Environ Microbiol. 2005; 71(11):7019-28. PMC: 1287694. DOI: 10.1128/AEM.71.11.7019-7028.2005. View

Taylor M, Radax R, Steger D, Wagner M . Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev. 2007; 71(2):295-347. PMC: 1899876. DOI: 10.1128/MMBR.00040-06. View

Janssen P, Yates P, Grinton B, Taylor P, Sait M . Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. Appl Environ Microbiol. 2002; 68(5):2391-6. PMC: 127570. DOI: 10.1128/AEM.68.5.2391-2396.2002. View

Radwan M, Hanora A, Zan J, Mohamed N, Abo-Elmatty D, Abou-El-Ela S . Bacterial community analyses of two Red Sea sponges. Mar Biotechnol (NY). 2009; 12(3):350-60. DOI: 10.1007/s10126-009-9239-5. View

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9. PMC: 3203626. DOI: 10.1093/molbev/msr121. View

Thomas T, Kavlekar D, LokaBharathi P . Marine drugs from sponge-microbe association--a review. Mar Drugs. 2010; 8(4):1417-68. PMC: 2866492. DOI: 10.3390/md8041417. View

Chun J, Goodfellow M . A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Bacteriol. 1995; 45(2):240-5. DOI: 10.1099/00207713-45-2-240. View

Luter H, Whalan S, Webster N . Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl Environ Microbiol. 2010; 76(17):5736-44. PMC: 2935071. DOI: 10.1128/AEM.00653-10. View

Zhang L, Xi L, Ruan J, Huang Y . Micromonospora yangpuensis sp. nov., isolated from a sponge. Int J Syst Evol Microbiol. 2011; 62(Pt 2):272-278. DOI: 10.1099/ijs.0.029439-0. View

10.

Kim T, Hewavitharana A, Shaw P, Fuerst J . Discovery of a new source of rifamycin antibiotics in marine sponge actinobacteria by phylogenetic prediction. Appl Environ Microbiol. 2006; 72(3):2118-25. PMC: 1393243. DOI: 10.1128/AEM.72.3.2118-2125.2006. View

11.

Abdelmohsen U, Pimentel-Elardo S, Hanora A, Radwan M, Abou-El-Ela S, Ahmed S . Isolation, phylogenetic analysis and anti-infective activity screening of marine sponge-associated actinomycetes. Mar Drugs. 2010; 8(3):399-412. PMC: 2857355. DOI: 10.3390/md8030399. View

12.

Giovannoni S, Stingl U . The importance of culturing bacterioplankton in the 'omics' age. Nat Rev Microbiol. 2007; 5(10):820-6. DOI: 10.1038/nrmicro1752. View

13.

Cassler M, Peterson C, Ledger A, Pomponi S, Wright A, Winegar R . Use of real-time qPCR to quantify members of the unculturable heterotrophic bacterial community in a deep sea marine sponge, Vetulina sp. Microb Ecol. 2007; 55(3):384-94. DOI: 10.1007/s00248-007-9283-5. View

14.

Thomas T, Rusch D, DeMaere M, Yung P, Lewis M, Halpern A . Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis. ISME J. 2010; 4(12):1557-67. DOI: 10.1038/ismej.2010.74. View

15.

Zhang H, Lee Y, Zhang W, Lee H . Culturable actinobacteria from the marine sponge Hymeniacidon perleve: isolation and phylogenetic diversity by 16S rRNA gene-RFLP analysis. Antonie Van Leeuwenhoek. 2006; 90(2):159-69. DOI: 10.1007/s10482-006-9070-1. View

16.

Sharp K, Eam B, Faulkner D, Haygood M . Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol. 2006; 73(2):622-9. PMC: 1796987. DOI: 10.1128/AEM.01493-06. View

17.

Lang S, Beil W, Tokuda H, Wicke C, Lurtz V . Improved production of bioactive glucosylmannosyl-glycerolipid by sponge-associated Microbacterium species. Mar Biotechnol (NY). 2004; 6(2):152-6. DOI: 10.1007/s10126-003-0009-5. View

18.

Schneemann I, Nagel K, Kajahn I, Labes A, Wiese J, Imhoff J . Comprehensive investigation of marine Actinobacteria associated with the sponge Halichondria panicea. Appl Environ Microbiol. 2010; 76(11):3702-14. PMC: 2876447. DOI: 10.1128/AEM.00780-10. View

19.

Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S . Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol. 2009; 69(1):113-24. DOI: 10.1111/j.1574-6941.2009.00688.x. View

20.

Webster N, Wilson K, Blackall L, Hill R . Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol. 2001; 67(1):434-44. PMC: 92596. DOI: 10.1128/AEM.67.1.434-444.2001. View