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

Marine Biotechnology

Volumn 14, Issue 3, 2012, Pages 270-280

  Hodges, Tyler W ^a,c   Slattery, Marc ^b   Olson, Julie B ^a  

^a UNIVERSITY OF ALABAMA   (United States)

^b UNIVERSITY OF MISSISSIPPI   (United States)

^c WILLIAM CAREY UNIVERSITY   (United States)

Author keywords

Actinomycetes; Marine; NRPS; PKS; Solwaraspora

Indexed keywords

ACTINOMYCETES; MARINE; NRPS; PKS; SOLWARASPORA;

ANOXIC SEDIMENTS; CAVES; GENES; METABOLITES; POLYMERASE CHAIN REACTION; REEFS; SEDIMENTOLOGY;

BACTERIA;

NONRIBOSOMAL PEPTIDE SYNTHETASE; PEPTIDE SYNTHASE; POLYKETIDE SYNTHASE;

BIOTECHNOLOGY; CAVE SYSTEM; CORAL REEF; GENETIC ANALYSIS; GEOGRAPHICAL VARIATION; HYPOTHESIS TESTING; LIGHT EFFECT; MARINE ENVIRONMENT; MARINE SEDIMENT; OPEN OCEAN; SECONDARY METABOLITE; SPONGE;

ACTINOBACTERIA; ACTINOMYCETALES; ARTICLE; CAVE; CLASSIFICATION; CORAL REEF; GENETICS; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PHYSIOLOGY; SEA; SEDIMENT; SPECIES DIFFERENCE;

ACTINOBACTERIA; ACTINOMYCETALES; CAVES; CORAL REEFS; GEOLOGIC SEDIMENTS; MULTIGENE FAMILY; OCEANS AND SEAS; PEPTIDE SYNTHASES; POLYKETIDE SYNTHASES; SPECIES SPECIFICITY;

BAHAMAS;

ACTINOBACTERIA; ACTINOBACTERIA (CLASS); ANTHOZOA; SOLWARASPORA; STREPTOMYCES;

EID: 84859424184     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-011-9410-7     Document Type: Article

References (60)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. Das A, Khosla C (2009) Biosynthesis of aromatic polyketides in bacteria. Acc Chem Res 42: 631-639.
10. 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.
11. 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.
12. 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.
13. 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.
14. Fichez R (1990) Decrease in allochthonous organic inputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia 207: 61-69.
15. Fichez R (1991a) Benthic oxygen uptake and carbon cycling under aphotic and resource-limiting conditions in a submarine cave. Mar Biol 110: 137-143.
16. 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.
17. 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.
18. 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.
19. 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.
20. Gontang EA, Fenical W, Jensen PR (2007) Phylogenetic diversity of gram-positive bacteria cultured from marine sediments. Appl Environ Microbiol 73: 3272-3282.
21. 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.
22. 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.
23. Hill RT, Peraud O, Hamann MT and Kasanah N (2003) Manzamine-producing actinomycetes. United States of America Patent US 20050244938 A1.
24. 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.
25. 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.
26. Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments. Appl Environ Microbiol 57: 1102-1108.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272: 1953-1955.
49. Schoemaker HE, Mink D, Wubbolts MG (2003) Dispelling the myths-biocatalysis in industrial synthesis. Science 299: 1694-1697.
50. Seymour JR, Humphreys WF, Mitchell JG (2007) Stratification of the microbial community inhabiting an anchialine sinkhole. Aquat Microb Ecol 50: 11-24.
51. Shen B (2003) Polyketide biosynthesis beyond the type I, II and III polyketide synthase paradigms. Curr Opin Chem Biol 7: 285-295.
52. Sket B (1996) The ecology of anchihaline caves. Trends Ecol Evol 11: 221-225.
53. 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.
54. Smith JL, Sherman DH (2008) An enzyme assembly line. Science 321: 1304-1305.
55. Swofford DL (2003) Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland, MA.
56. Walsh CT (2004) Polyketide and nonribosomal peptide antibiotics: modularity and versatility. Science 303: 1805-1810.
57. Walsh CT (2008) The chemical versatility of natural-product assembly lines. Acc Chem Res 41: 4-10.
58. Weyland H (1981) Distribution of actinomycetes on the sea floor. Zentralbl Bakteriol Suppl 11: 185-193.
59. Wright LF, Hopwood DA (1976) Actinorhodin is a chromosomally-determined antibiotic in Streptomyces coelicolor A3(2). J Gen Microbiol 96: 289-297.
60. Zhang C, Kim S-K (2010) Research and application of marine microbial enzymes: status and prospects. Mar Drugs 8: 1920-1934.