Skip to main content

Advertisement

SpringerLink
Log in

Unique Actinomycetes from Marine Caves and Coral Reef Sediments Provide Novel PKS and NRPS Biosynthetic Gene Clusters

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

In the ever-expanding search for novel bioactive molecules and enzymes, marine actinomycetes have proven to be a productive source. While open reef sediment and sponge-associated actinomycetes have been extensively examined, their marine cave counterparts remain unevaluated. Anchialine cave systems in the Bahamas offered an ideal setting to evaluate the occurrence and variation within sediment-associated actinomycete communities. While in close geographical proximity to open reef environments, these systems provide a specialized environmental niche devoid of light and direct exposure to nutrient input. In the present study, selective isolation techniques and molecular methods were used to test the hypothesis that variable distribution of actinomycetes and secondary metabolite gene clusters occur between open reef and marine cave systems. The results indicated that differences exist within the culturable sediment-associated actinomycete communities between marine caves and open reef systems, with members of the genus Streptomyces dominating cultures from open reef sediments and a more diverse suite of actinomycetes isolated from marine cave sediment samples. Within the cave isolates, members of the proposed genus Solwaraspora were the most represented. Based on PKS- and NRPS-gene-targeted PCR amplification and sequencing, geographic variation in the occurrence of these biosynthetic pathways was also observed. These findings indicate that marine cave systems are a lucrative source in the search for novel secondary metabolite producers with biotechnological applications and that environmental and geographic factors likely affect the occurrence of these biosynthetic pathways.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Airoldi L, Cinelli F (1996) Variability of fluxes of particulate material in a submarine cave with chemolithoautotrophic inputs of organic carbon. Mar Ecol Prog Ser 139:205–217

    Article  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Arisawa A, Matsufuji M, Nakashima T, Dobashi K, Isshiki K, Yoshioka T, Yamada S, Momose H, Taguchi S (2002) Streptomyces serine protease (DHP-A) as a new biocatalyst capable of forming chiral intermediates of 1,4-dihydropyridine calcium antagonists. Appl Environ Microbiol 68:2716–2725

    Article  PubMed  CAS  Google Scholar 

  • Ayer SW, McInnes AG, Thibault P, Walter JA, Doull JL, Parnell T, Vining LC (1991) Jadomycin, a novel 8H-benz[b]oxazolo[3,2-f]phenanthridine antibiotic from Streptomyces venezuelae ISP5230. Tetrahedron Lett 32:6301–6304

    Article  CAS  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  CAS  Google Scholar 

  • Canganella F, Bianconi G, Kato C, Gonzalez J (2007) Microbial ecology of submerged marine caves and holes characterized by high levels of hydrogen sulphide. Rev Environ Sci Biotechnol 6:61–70

    Article  CAS  Google Scholar 

  • Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100(Suppl 2):14555–14561

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Tseng CC, Hubbard BK, Walsh CT (2001) Glycopeptide antibiotic biosynthesis: enzymatic assembly of the dedicated amino acid monomer (S)-3,5-dihydroxyphenylglycine. Proc Natl Acad Sci USA 98:14901–14906

    Article  PubMed  CAS  Google Scholar 

  • Das A, Khosla C (2009) Biosynthesis of aromatic polyketides in bacteria. Acc Chem Res 42:631–639

    Article  PubMed  CAS  Google Scholar 

  • Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC (2004) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic “Epsilonproteobacteria”. FEMS Microbiol Ecol 51:31–53

    Article  PubMed  CAS  Google Scholar 

  • Eustaquio AS, Pojer F, Noel JP, Moore BS (2008) Discovery and characterization of a marine bacterial SAM-dependent chlorinase. Nat Chem Biol 4:69–74

    Article  PubMed  CAS  Google Scholar 

  • Feling RH, Buchanan GO, Mincer TJ, Kauffman CA, Jensen PR, Fenical W (2003) Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora. Angew Chem 115:369–371

    Article  Google Scholar 

  • Fenical W, Jensen PR, Palladino MA, Lam KS, Lloyd GK, Potts BC (2009) Discovery and development of the anticancer agent salinosporamide A (NPI-0052). Bioorg Med Chem 17:2175–2180

    Article  PubMed  CAS  Google Scholar 

  • Fichez R (1990) Decrease in allochthonous organic inputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia 207:61–69

    Article  Google Scholar 

  • Fichez R (1991a) Benthic oxygen uptake and carbon cycling under aphotic and resource-limiting conditions in a submarine cave. Mar Biol 110:137–143

    Article  Google Scholar 

  • Fichez R (1991b) Composition and fate of organic matter in submarine cave sediments; implications for the biogeochemical cycle of organic carbon. Oceanol Acta 14:369–377

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Foldes M, Munro R, Sorrell TC, Shanker S, Toohey M (1983) In-vitro effects of vancomycin, rifampicin, and fusidic acid, alone and in combination, against methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 11:21–26

    Article  PubMed  CAS  Google Scholar 

  • Gili JM, Riera T, Zabala M (1986) Physical and biological gradients in a submarine cave on the Western Mediterranean coast (north-east Spain). Mar Biol 90:291–297

    Article  Google Scholar 

  • Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272–3282

    Article  PubMed  CAS  Google Scholar 

  • Gontang EA, Gaudencio SP, Fenical W, Jensen PR (2010) Sequence-based analysis of secondary-metabolite biosynthesis in marine Actinobacteria. Appl Environ Microbiol 76:2487–2499

    Article  PubMed  CAS  Google Scholar 

  • Henkel T, Rohr J, Beale JM, Schwenen L (1990) Landomycins, new angucycline antibiotics from Streptomyces sp. I. Structural studies on landomycins A–D. J Antibiot (Tokyo) 43:492–503

    Article  CAS  Google Scholar 

  • Hill RT, Peraud O, Hamann MT and Kasanah N (2003) Manzamine-producing actinomycetes. United States of America Patent US 20050244938 A1

  • Humphreys WF (1999) Physico-chemical profile and energy fixation in Bundera Sinkhole, ananchialine remiped habitat in north-western Australia. J Roy Soc West Aust 82:89–98

    Google Scholar 

  • Ichinose K, Bedford DJ, Tornus D, Bechthold A, Bibb MJ, Revill WP, Floss HG, Hopwood DA (1998) The granaticin biosynthetic gene cluster of Streptomyces violaceoruber Tü22: sequence analysis and expression in a heterologous host. Chem Biol 5:647–659

    Article  PubMed  CAS  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  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jiang S, Li X, Zhang L, Sun W, Dai S, Xie L, Liu Y, Lee K (2008) Culturable Actinobacteria isolated from marine sponge Iotrochota sp. Mar Biol 153:945–952

    Article  CAS  Google Scholar 

  • Kantola J, Kunnari T, Mantsala P, Ylihonko K (2003) Expanding the scope of aromatic polyketides by combinatorial biosynthesis. Comb Chem High Throughput Screen 6:501–512

    PubMed  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  PubMed  CAS  Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959

    Article  PubMed  CAS  Google Scholar 

  • Magarvey NA, Keller JM, Bernan V, Dworkin M, Sherman DH (2004) Isolation and characterization of novel marine-derived actinomycete taxa rich in bioactive metabolites. Appl Environ Microbiol 70:7520–7529

    Article  PubMed  CAS  Google Scholar 

  • Maldonado LA, Fenical W, Jensen PR, Kauffman CA, Mincer TJ, Ward AC, Bull AT, Goodfellow M (2005) Salinispora arenicola gen. nov., sp. nov. and Salinispora tropica sp. nov., obligate marine actinomycetes belonging to the family Micromonosporaceae. Int J Syst Evol Microbiol 55:1759–1766

    Article  PubMed  CAS  Google Scholar 

  • Maldonado LA, Stach J, Ward A, Bull A, Goodfellow M (2008) Characterisation of micromonosporae from aquatic environments using molecular taxonomic methods. Antonie Van Leeuwenhoek 94:289–298

    Article  PubMed  CAS  Google Scholar 

  • Maldonado LA, Fragoso-Yáñez D, Pérez-García A, Rosellón-Druker J, Quintana E (2009) Actinobacterial diversity from marine sediments collected in Mexico. Antonie van Leeuwenhoek 95:111–120

    Article  PubMed  CAS  Google Scholar 

  • Mayer AMS, Glaser KB, Cuevas C, Jacobs RS, Kem W, Little RD, McIntosh JM, Newman DJ, Potts BC, Shuster DE (2010) The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol Sci 31:255–265

    Article  PubMed  CAS  Google Scholar 

  • McLeod MP, Warren RL, Hsiao WW, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103:15582–15587

    Article  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  Google Scholar 

  • Miller ED, Kauffman CA, Jensen PR, Fenical W (2006) Piperazimycins: cytotoxic hexadepsipeptides from a marine-derived bacterium of the genus Streptomyces. J Org Chem 72:323–330

    Article  Google Scholar 

  • Mincer TJ, Jensen PR, Kauffman 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  CAS  Google Scholar 

  • Pfeifer V, Nicholson GJ, Ries J, Recktenwald J, Schefer AB, Shawky RM, Schroder J, Wohlleben W, Pelzer S (2001) A polyketide synthase in glycopeptide biosynthesis: the biosynthesis of the non-proteinogenic amino acid (S)-3,5-dihydroxyphenylglycine. J Biol Chem 276:38370–38377

    Article  PubMed  CAS  Google Scholar 

  • Piecq M, Dehottay P, Biot A, Dusart J (1994) Cloning and nucleotide sequence of a region of the Kibdelosporangium aridum genome homologous to polyketide biosynthetic genes. DNA Seq 4:219–229

    PubMed  CAS  Google Scholar 

  • Pohlman J, Iliffe T, Cifuentes L (1997) A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Mar Ecol Prog Ser 155:17–27

    Article  CAS  Google Scholar 

  • Prudhomme J, McDaniel E, Ponts N, Bertani S, Fenical W, Jensen P, Le Roch K (2008) Marine actinomycetes: a new source of compounds against the human malaria parasite. PLoS One 3:e2335

    Article  PubMed  Google Scholar 

  • Ramesh S, Mathivanan N (2009) Screening of marine actinomycetes isolated from the Bay of Bengal, India for antimicrobial activity and industrial enzymes. World J Microb Biot 25:2103–2111

    Article  CAS  Google Scholar 

  • Sarabia F, Chammaa S, Ruiz AS, Ortiz LM, Herrera FJL (2004) Chemistry and biology of cyclic depsipeptides of medicinal and biological interest. Curr Med Chem 11:1309–1332

    PubMed  CAS  Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955

    Article  PubMed  CAS  Google Scholar 

  • Schoemaker HE, Mink D, Wubbolts MG (2003) Dispelling the myths—biocatalysis in industrial synthesis. Science 299:1694–1697

    Article  PubMed  CAS  Google Scholar 

  • Seymour JR, Humphreys WF, Mitchell JG (2007) Stratification of the microbial community inhabiting an anchialine sinkhole. Aquat Microb Ecol 50:11–24

    Article  Google Scholar 

  • Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295

    Article  PubMed  CAS  Google Scholar 

  • Sket B (1996) The ecology of anchihaline caves. Trends Ecol Evol 11:221–225

    Article  PubMed  CAS  Google Scholar 

  • Slattery M, Gochfeld DJ, Iliffe TM, Kakuk B, Kelly M (2002) Biodiversity and competitive interactions of cave sponges in the Bahamas. Boll Musei Ist Biolog 66:184

    Google Scholar 

  • Smith JL, Sherman DH (2008) An enzyme assembly line. Science 321:1304–1305

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2003) Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303:1805–1810

    Article  PubMed  CAS  Google Scholar 

  • Walsh CT (2008) The chemical versatility of natural-product assembly lines. Acc Chem Res 41:4–10

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Wright LF, Hopwood DA (1976) Actinorhodin is a chromosomally-determined antibiotic in Streptomyces coelicolor A3(2). J Gen Microbiol 96:289–297

    PubMed  CAS  Google Scholar 

  • Zhang C, Kim S-K (2010) Research and application of marine microbial enzymes: status and prospects. Mar Drugs 8:1920–1934

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the staff of the Caribbean Marine Research Center (CMRC) for housing, facilities, and assistance with sample collection. We also thank D. Gochfeld for assistance in sample collection and C. Easson for assistance with figures. This project was supported by NOAA/NIUST National Institute for Undersea Science and Technology grant NA16RU1496 to J.B.O.

Author information

Author notes

  1. Tyler W. Hodges

    Present address: William Carey University, 498 Tuscan Avenue, Box 203, Hattiesburg, MS, 39401, USA

Authors and Affiliations

  1. Department of Biological Sciences, The University of Alabama, 1325 SEC Building, Campus Box 870344, Tuscaloosa, AL, 35487, USA

    Tyler W. Hodges & Julie B. Olson

  2. Department of Pharmacognosy, School of Pharmacy, The University of Mississippi, Oxford, MS, 38677, USA

    Marc Slattery

Authors
  1. Tyler W. Hodges
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marc Slattery
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie B. Olson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julie B. Olson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hodges, T.W., Slattery, M. & Olson, J.B. Unique Actinomycetes from Marine Caves and Coral Reef Sediments Provide Novel PKS and NRPS Biosynthetic Gene Clusters. Mar Biotechnol 14, 270–280 (2012). https://doi.org/10.1007/s10126-011-9410-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-011-9410-7

Keywords

Search

Navigation