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Detection of polyketide synthase and nonribosomal peptide synthetase biosynthetic genes from antimicrobial coral-associated actinomycetes

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Abstract

The diversity and properties of actinobacteria, predominant residents in coral holobionts, have been rarely documented. In this study, we aimed to explore the species diversity, antimicrobial activities and biosynthetic potential of culturable actinomycetes within the tissues of the scleractinian corals Porites lutea, Galaxea fascicularis and Acropora millepora from the South China Sea. A total of 70 strains representing 13 families and 15 genera of actinobacteria were isolated. The antimicrobial activity and biosynthetic potential of fifteen representative filamentous actinomycetes were estimated. Crude fermentation extracts of 6 strains exhibited comparable or greater activities against Vibrio alginolyticus than ciprofloxacin. Seven of the 15 actinomycetes strains possess type I polyketide synthases (PKS-I) and/or nonribosomal peptide synthetases (NRPS) genes. Nine tested strains possess type II polyketide synthases (PKS-II). Phylogenetic analysis based on 16S rRNA gene sequences indicated that these PKS and NRPS gene screening positive strains belong to genera Nocardiopsis, Pseudonocardia, Streptomyces, Micromonospora, Amycolatopsis and Prauserella. One PKS-I and four NRPS fragments showed <70 % similarity to their closest relatives, which suggested the novelty of these genes. This study helps uncover the genetic capacity of stony coral-associated actinomycetes to produce bioactive molecules.

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References

  • 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  CAS  PubMed  Google Scholar 

  • Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8:557–563

    Article  CAS  PubMed  Google Scholar 

  • Barott KL, Rodriguez-Brito B, Janouškovec J, Marhaver KL, Smith JE, Keeling P, Rohwer FL (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192–1204

    Article  CAS  PubMed  Google Scholar 

  • Ben-Dov E, Ben Yosef DZ, Pavlov V, Kushmaro A (2009) Corynebacterium maris sp. nov., a marine bacterium isolated from the mucus of the coral Fungia granulose. Int J Syst Evol Microbiol 59:2458–2463

    Article  CAS  PubMed  Google Scholar 

  • Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 65:385–395

    Article  PubMed  Google Scholar 

  • Bergh S, Uhlén M (1992) Cloning, analysis, and heterologous expression of a polyketide synthase gene cluster of Streptomyces curacoi. Biotechnol Appl Biochem 15:80–89

    Article  CAS  PubMed  Google Scholar 

  • Blanco G, Brian P, Pereda A, Méndez C, Salas JA, Chater KF (1993) Hybridization and DNA sequence analyses suggest an early evolutionary divergence of related biosynthetic gene sets encoding polyketide antibiotics and spore pigments in Streptomyces spp. Gene 130:107–116

    Article  CAS  PubMed  Google Scholar 

  • Cardenas A, Rodriguez-R LM, Pizarro V, Cadavid LF, Arevalo-Ferro C (2012) Shifts in bacterial communities of two Caribbean reef-building coral species affected by white plague disease. ISME J 6:502–512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cervino JM, Thompson FL, Gomez-Gil B, Lorence EA, Goreau TJ, Hayes RL, Winiarski-Cervino KB, Smith GW, Hughen K, Bartels E (2008) The Vibrio core group induces yellow band disease in Caribbean and Indo-Pacific reef-building corals. J Appl Microbiol 105:1658–1671

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Huang X, Zhou X, Bai L, He J, Jeong KJ, Lee SY, Deng Z (2003) Organizational and mutational analysis of a complete FR-008/candicidin gene cluster encoding a structurally related polyene complex. Chem Biol 10:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Chiu JMY, Li S, Li A, Po B, Zhang R, Shin PKS, Qiu JW (2012) Bacteria associated with skeletal tissue growth anomalies in the coral Platygyra carnosus. FEMS Microbiol Ecol 79:380–391

    Article  CAS  PubMed  Google Scholar 

  • Davis NK, Chater KF (1990) Spore colour in Streptomyces coelicolor A3(2) involves the developmentally regulated synthesis of a compound biosynthetically related to polyketide antibiotics. Mol Microbiol 4:1679–1691

    Article  CAS  PubMed  Google Scholar 

  • Gontang EA, Gaudêncio SP, Fenical W, Jensen PR (2010) Sequence-Based Analysis of Secondary-Metabolite Biosynthesis in Marine Actinobacteria. Appl Environ Microbiol 76:2487–2499

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Grimm A, Madduri K, Ali A, Hutchinson CR (1994) Characterization of the Streptomyces peucetius ATCC 29050 genes encoding doxorubicin polyketide synthase. Gene 151:1–10

    Article  CAS  PubMed  Google Scholar 

  • Hopkins DW, Macnaughton SJ, O’Donnell AG (1991) A dispersion and differential centrifugation technique for representatively sampling microorganisms from soil. Soil Biol Biochem 23:217–225

    Article  Google Scholar 

  • Jensen PR, Williams PG, Oh DC, Zeigler L, Fenical W (2007) Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl Environ Microbiol 73:1146–1152

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kageyama A, Takahashi Y, Yasumoto-Hirose M, Kasai H, Shizuri Y, Omura S (2007) Janibacter corallicola sp. nov., isolated from coral in Palau. J Gen Appl Microbiol 53:185–189

    Article  CAS  PubMed  Google Scholar 

  • Kelman D, Kashman Y, Hill RT, Rosenberg E, Loya Y (2009) Chemical warfare in the sea: the search for antibiotics from Red Sea corals and sponges. Pure Appl Chem 81:1113–1121

    Article  CAS  Google Scholar 

  • Kim TK, Hewavitharana AK, Shaw PN, Fuerst JA (2006) Discovery of a new source of rifamycin antibiotics in marine sponge actinobacteria by phylogenetic prediction. Appl Environ Microbiol 72:2118–2125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, 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 

  • Kobayashi J, Ishibashi M (1993) Bioactive metabolites of symbiotic marine microorganisms. Chem Rev 93:1753–1769

    Article  CAS  Google Scholar 

  • Lampert Y, Kelman D, Dubinsky Z, Nitzan Y, Hill RT (2006) Diversity of culturable bacteria in the mucus of the Red Sea coral Fungia scutaria. FEMS Microbiol Ecol 58:99–108

    Article  CAS  PubMed  Google Scholar 

  • Lane AL, Moore BS (2011) A sea of biosynthesis: marine natural products meet the molecular age. Nat Prod Rep 28:411–428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li ZY (2009) Advances in marine microbial symbionts in the China sea and related pharmaceutical metabolites. Mar Drugs 7:113–129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li WJ, Xu P, Schumann P, Zhang YQ, Pukall R, Xu LH, Stackebrandt E, Jiang CL (2007) Georgenia ruanii sp. nov., a novel actinobacterium isolated from forest soil in Yunnan (China), and emended description of the genus Georgenia. Int J Syst Evol Microbiol 57:1424–1428

    Article  PubMed  Google Scholar 

  • Liu ZF, Huang W, Li JR, Wang PX, Wang RJ, Yu KF, Zhao JX (2009) Sedimentology. In: Wang P, Li Q (eds) The south China sea, developments in paleoenvironmental research. Springer Science + Business Media B. V, Dordrecht, pp 229–236

    Google Scholar 

  • Lombó F, Braña AF, Méndez C, Salas JA (1999) The mithramycin gene cluster of Streptomyces argillaceus contains a positive regulatory gene and two repeated DNA sequences that are located at both ends of the cluster. J Bacteriol 181:642–647

    PubMed Central  PubMed  Google Scholar 

  • Lykidis A, Mavromatis K, Ivanova N, Anderson I, Land M, DiBartolo G, Martinez M, Lapidus A, Lucas S, Copeland A, Richardson P, Wilson DB, Kyrpides N (2007) Genome sequence and analysis of the soil cellulolytic actinomycete Thermobifida fusca YX. J Bacteriol 189:2477–2486

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mearns-Spragg A, Bregu M, Boyd KG, Burgess JG (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Lett Appl Microbiol 27:142–146

    Article  CAS  PubMed  Google Scholar 

  • Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6

    Article  PubMed  Google Scholar 

  • Metsä-Ketelä M, Halo L, Munukka E, Hakala J, Mäntsälä 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 Central  PubMed  Google Scholar 

  • Nithyanand P, Pandian SK (2009) Phylogenetic characterization of culturable bacterial diversity associated with the mucus and tissue of the coral Acropora digitifera from the Gulf of Mannar. FEMS Microbiol Ecol 69:384–394

    Article  CAS  PubMed  Google Scholar 

  • Nithyanand P, Thenmozhi R, Rathna J, Pandian SK (2010) Inhibition of Streptococcus pyogenes biofilm formation by coral-associated actinomycetes. Curr Microbiol 60:454–460

    Article  CAS  PubMed  Google Scholar 

  • Nithyanand P, Manju S, Pandian SK (2011) Phylogenetic characterization of culturable actinomycetes associated with the mucus of the coral Acropora digitifera from Gulf of Mannar. FEMS Microbiol Lett 314:112–118

    Article  CAS  PubMed  Google Scholar 

  • Räty K, Kantola J, Hautala A, Hakala J, Ylihonko K, Mäntsälä P (2002) Cloning and characterization of Streptomyces galilaeus aclacinomycins polyketide synthase (PKS) cluster. Gene 293:115–122

    Article  PubMed  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  • Rypien KL, Ward JR, Azam F (2010) Antagonistic interactions among coral-associated bacteria. Environ Microbiol 12:28–39

    Article  CAS  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 

  • Schneemann I, Nagel K, Kajahn I, Labes A, Wiese J, Imhoff JF (2010) Comprehensive investigation of marine actinobacteria associated with the sponge Halichondria panicea. Appl Environ Microbiol 76:3702–3714

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380

    Article  CAS  PubMed  Google Scholar 

  • Sitachitta N, Gadepalli M, Davidson BS (1996) New α-pyrone-containing metabolites from a marine-derived Actinomycete. Tetrahedron 52:8073–8080

    Article  CAS  Google Scholar 

  • Sun W, Peng C, Zhao Y, Li Z (2012) Functional gene-guided discovery of type II polyketides from culturable actinomycetes associated with soft coral Scleronephthya sp. PLoS One 7:e42847

    Article  CAS  PubMed Central  PubMed  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 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA, Angly F, Dinsdale E, Kelly L, Rohwer F (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163

    Article  CAS  Google Scholar 

  • Yang S, Sun W, Tang C, Jin L, Zhang F, Li Z (2013) Phylogenetic diversity of actinobacteria associated with soft coral Alcyonium gracllimum and stony coral Tubastraea coccinea in the East China Sea. Microb Ecol 66:189–199

    Article  PubMed  Google Scholar 

  • Zhang S, Zhang C, Tian X, Wang F, Li J (2010) The study of diversities of marine microbes in China. Bull Chin Acad Sci 4:228–234

    Google Scholar 

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Acknowledgments

Tropical Marine Biological Research Station in Hainan is gratefully acknowledged for collecting coral samples. We thank Dr. Guangtao Zhang and Dr. Yiguang Zhu for helpful discussions. This research was supported by the Pearl River Nova Program of Guangzhou (No. 2014J2200075), the National Natural Science Foundation of China (No. 41106139, 41230962), Administration of Ocean and Fisheries of Guangdong Province (No. GD2012-D01-002) and the Knowledge Innovation Program of the Chinese Academy of Sciences (No. SQ201301).

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  1. CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, RNAM Center for Marine Microbiology, Guangdong Key Laboratory of Marine Materia Medica, South China Sea Institute of Oceanology, Chinese Academy of Sciences, 164 West Xingang Road, Guangzhou, 510301, People’s Republic China

    Jie Li, Jun-De Dong, Jian Yang, Xiong-Ming Luo & Si Zhang

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  1. Jie Li
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  2. Jun-De Dong
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Correspondence to Si Zhang.

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Li, J., Dong, JD., Yang, J. et al. Detection of polyketide synthase and nonribosomal peptide synthetase biosynthetic genes from antimicrobial coral-associated actinomycetes. Antonie van Leeuwenhoek 106, 623–635 (2014). https://doi.org/10.1007/s10482-014-0233-1

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