Actinomycetes from red sea sponges: Sources for chemical and phylogenetic diversity

Marine Drugs

Volumn 12, Issue 5, 2014, Pages 2771-2789

  Abdelmohsen, Usama Ramadan ^a,c   Yang, Chen ^b   Horn, Hannes ^a   Hajjar, Dina ^b   Ravasi, Timothy ^b   Hentschel, Ute ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c Minia University   (Egypt)

Author keywords

Actinomycetes; Bioactivity; NRPS; PKS I; PKS II; Red sea; Sponges

Indexed keywords

NATURAL PRODUCT; NONRIBOSOMAL PEPTIDE SYNTHETASE; POLYKETIDE SYNTHASE; POLYKETIDE SYNTHASE 1; POLYKETIDE SYNTHASE 2; RNA 16S; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; ANTIPROTOZOAL AGENT; ANTITRYPANOSOMAL AGENT; PROTEINASE INHIBITOR;

16S RRNA GENE; ACTINOBACTERIA; ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; ANTILEISHMANIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTITRYPANOSOMAL ACTIVITY; ARTICLE; BACILLUS; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CONTROLLED STUDY; DRUG SCREENING; ENZYMATIC ASSAY; ESCHERICHIA COLI K 12; FUSARIUM; GENE SEQUENCE; GENETIC VARIABILITY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; KOCURIA; LEISHMANIA MAJOR; MYCOBACTERIUM; NOCARDIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; RED SEA SPONGE; RHODOCOCCUS; SAUDI ARABIA; SEQUENCE HOMOLOGY; SPECIES CULTIVATION; SPONGE (PORIFERA); TRYPANOSOMA BRUCEI; WEST NILE FLAVIVIRUS; ANIMAL; BACTERIA; BIODIVERSITY; BIOSYNTHESIS; CHEMISTRY; CLASSIFICATION; DRUG EFFECTS; FUNGUS; GENETICS; INDIAN OCEAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; TRYPANOSOMA BRUCEI BRUCEI;

ACTINOBACTERIA; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIPROTOZOAL AGENTS; BACTERIA; BIODIVERSITY; FUNGI; INDIAN OCEAN; MICROBIAL SENSITIVITY TESTS; PHYLOGENY; PORIFERA; PROTEASE INHIBITORS; SAUDI ARABIA; TRYPANOCIDAL AGENTS; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84901429529     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12052771     Document Type: Article

References (71)

1. Hentschel, U.; Piel, J.; Degnan, S.M.; Taylor, M.W. Genomic insights into the marine sponge microbiome. Nature 2012, 10, 641-654.
2. Van Soest, R.W.; Boury-Esnault, N.; Vacelet, J.; Dohrmann, M.; Erpenbeck, D.; de Voogd, N.J.; Santodomingo, N.; Vanhoorne, B.; Kelly, M.; Hooper, J.N. Global diversity of sponges (Porifera). PLoS One 2012, 7, e35105.
3. Schmitt, S.; Tsai, P.; Bell, J.; Fromont, J.; Ilan, M.; Lindquist, N.; Perez, T.; Rodrigo, A.; Schupp, P.J.; Vacelet, J.; et al. Assessing the complex sponge microbiota: Core, variable and species-specific bacterial communities in marine sponges. ISME J. 2012, 6, 564-576.
4. Belarbi el, H.; Contreras Gomez, A.; Chisti, Y.; Garcia Camacho, F.; Molina Grima, E. Producing drugs from marine sponges. Biotechnol. Adv. 2003, 21, 585-598.
5. Webster, N.S.; Taylor, M.W. Marine sponges and their microbial symbionts: Love and other relationships. Environ. Microbiol. 2012, 14, 335-346.
6. Hentschel, U.; Fieseler, L.; Wehrl, A.; Gernert, C.; Steinert, M.; Hacker, J.; Horn, M. Microbial diversity of marine sponges. In Sponges (Porifera); Müller, W.E.G., Ed.; Springer: Berlin, Germany, 2003; pp. 59-88.
7. Ventura, M.; Canchaya, C.; Tauch, A.; Chandra, G.; Fitzgerald, G.F.; Chater, K.F.; van Sinderen, D.; Genomics of Actinobacteria: Tracing the evolutionary history of an ancient phylum. Microbiol. Mol. Biol. Rev. 2007, 71, 495-548.
8. Goodfellow, M.; Williams, S.T. Ecology of actinomycetes. Annu. Rev. Microbiol. 1983, 37, 189-216.
9. Garrity, G.M.; Bell, J.A.; Lilburn, T.G. Taxonomic outline of the prokaryotes. In Bergey's Manual of Systematic Bacteriology; Gray, M.W., Burger, G., Lang, B.F., Eds.; Springer: New York, NY, USA, 2004; pp. 204-301.
10. Adegboye, M.F.; Babalola, O.O. Taxonomy and ecology of antibiotic producing actinomycetes Afr. J. Agric. Res. 2012, 15, 2255-2261.
11. Andrade, M.R.M.; Amaral, E.P.; Ribeiro, S.C.M.; Almeida, F.M.; Peres, T.V.; Lanes, V.; D'Imperio-Lima, M.R.; Lasunskaia, E.B. Pathogenic Mycobacterium bovis strains differ in their ability to modulate the proinflammatory activation phenotype of macrophages. BMC Microbiol. 2012, 12, 166; doi:10.1186/1471-2180-12-166.
12. Salem, H.; Kreutzer, E.; Sudakaran, S.; Kaltenpoth, M. Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ. Microbiol. 2013, 15, 1956-1968.
13. Sun, W.; Dai, S.; Jiang, S.; Wang, G.; Liu, G.; Wu, H.; Li, X. Culture-dependent and culture-independent diversity of Actinobacteria associated with the marine sponge Hymeniacidon perleve from the South China Sea. Anton Van Leeuwenhoek 2010, 98, 65-75.
14. Zhang, L.M.; Xi, L.J.; Ruan, J.S.; Huang, Y. Microbacterium marinum sp nov., isolated from deep-sea water. Syst. Appl. Microbiol. 2012, 35, 81-85.
15. Becerril-Espinosa, A.; Freel, K.C.; Jensen, P.R.; Soria-Mercado, I.E. Marine actinobacteria from the Gulf of California: Diversity, abundance and secondary metabolite biosynthetic potential. Antonie Van Leeuwenhoek 2013, 103, 809-819.
16. Sun, W.; Peng, C.S.; Zhao, Y.Y.; Li, Z.Y. Functional gene-guided discovery of type II polyketides from culturable actinomycetes associated with soft coral Scleronephthya sp. PLoS One 2012, 7, e42847.
17. Abdelmohsen, U.R.; Pimentel-Elardo, S.M.; Hanora, A.; Radwan, M.; Abou-El-Ela, S.H.; Ahmed, S.; Hentschel, U. Isolation, phylogenetic analysis and anti-infective activity screening of marine sponge-associated actinomycetes. Mar. Drugs 2010, 8, 399-412.
18. Wyche, T.P.; Hou, Y.P.; Vazquez-Rivera, E.; Braun, D.; Bugni, T.S. Peptidolipins B-F, antibacterial lipopeptides from an ascidian-derived Nocardia sp. J. Nat. Prod. 2012, 75, 735-740.
19. Zhang, H.; Lee, Y.K.; Zhang, W.; Lee, H.K. Culturable actinobacteria from the marine sponge Hymeniacidon perleve: Isolation and phylogenetic diversity by 16S rRNA gene-RFLP analysis. Anton Van Leeuwenhoek 2006, 90, 159-169. (Pubitemid 44268882)
20. Xi, L.; Ruan, J.; Huang, Y. Diversity and biosynthetic potential of culturable actinomycetes associated with marine sponges in the china seas. Int. J. Mol. Sci. 2012, 13, 5917-5932.
21. Lam, K.S. Discovery of novel metabolites from marine actinomycetes. Curr. Opin. Microbiol. 2006, 9, 245-251. (Pubitemid 43817620)
22. Thomas, T.R.A.; Kavlekar, D.P.; LokaBharathi, P.A. Marine drugs from sponge-microbe association-A Review. Mar. Drugs 2010, 8, 1417-1468.
23. Pimentel-Elardo, S.M.; Kozytska, S.; Bugni, T.S.; Ireland, C.M.; Moll, H.; Hentschel, U. Anti-parasitic compounds from Streptomyces sp. strains isolated from Mediterranean sponges. Mar. Drugs 2010, 8, 373-380.
24. Blunt, J.W.; Copp, B.R.; Keyzers, R.A.; Munro, M.H.; Prinsep, M.R. Marine natural products. Nat. Prod. Rep. 2013, 30, 237-323.
25. Abdelmohsen, U.R.; Szesny, M.; Othman, E.M.; Schirmeister, T.; Grond, S.; Stopper, H.; Hentschel, U. Antioxidant and anti-Protease activities of diazepinomicin from the sponge-associated Micromonospora strain RV115. Mar. Drugs 2012, 10, 2208-2221.
26. Bull, A.T.; Stach, J.E. Marine actinobacteria: New opportunities for natural product search and discovery. Trends Microbiol. 2007, 15, 491-499. (Pubitemid 350102189)
27. Solanki, R.; Khanna, M.; Lal, R. Bioactive compounds from marine actinomycetes. Indian J. Microbiol. 2008, 48, 410-431.
28. Subramani, R.; Aalbersberg, W. Marine actinomycetes: An ongoing source of novel bioactive metabolites. Microbiol. Res. 2012, 167, 571-580.
29. Fenical, W.; Jensen, P.R. Developing a new resource for drug discovery: Marine actinomycete bacteria. Nat. Chem. Biol. 2006, 2, 666-673. (Pubitemid 44764208)
30. Tiwari, K.; Gupta, R.K. Rare actinomycetes: A potential storehouse for novel antibiotics. Crit. Rev. Biotechnol. 2012, 32, 108-132.
31. Donadio, S.; Monciardini, P.; Sosio, M. Polyketide synthases and nonribosomal peptide synthetases: The emerging view from bacterial genomics. Nat. Prod. Rep. 2007, 24, 1073-1109.
32. Fieseler, L.; Hentschel, U.; Grozdanov, L.; Schirmer, A.; Wen, G.; Platzer, M.; Hrvatin, S.; Butzke, D.; Zimmermann, K.; Piel, J. Widespread occurrence and genomic context of unusually small polyketide synthase genes in microbial consortia associated with marine sponges. Appl. Environ. Microbiol. 2007, 73, 2144-2155. (Pubitemid 46649504)
33. Chen, Y.Q.; Ntai, I.; Ju, K.S.; Unger, M.; Zamdborg, L.; Robinson, S.J.; Doroghazi, J.R.; Labeda, D.P.; Metcalf, W.W.; Kelleher, N.L. A proteomic survey of nonribosomal peptide and polyketide biosynthesis in Actinobacteria. J. Proteome Res. 2012, 11, 85-94.
34. Plahn, O.; Baschek, B.; Badewien, T.H.; Walter, M.; Rhein, M. Importance of the Gulf of Aqaba for the formation of bottom water in the Red Sea. J. Geophys. Res. Ocean. 2002, 107, 22/1-22/18.
35. Ilan, M.; Gugel, J.; van Soest, R.W.M. Taxonomy, reproduction and ecology of new and known Red Sea sponges. Sarsia 2004, 89, 388-410.
36. Ngugi, D.K.; Antunes, A.; Brune, A.; Stingl, U. Biogeography of pelagic bacterioplankton across an antagonistic temperature-salinity gradient in the Red Sea. Mol. Ecol. 2012, 21, 388-405.
37. Radwan, M.; Hanora, A.; Zan, J.; Mohamed, N.M.; Abo-Elmatty, D.M.; Abou-El-Ela, S.H.; Hill, R.T. Bacterial community analyses of two Red Sea sponges. Mar. Biotechnol. 2010, 12, 350-360.
38. Vicente, J.; Stewart, A.; Song, B.; Hill, R.; Wright, J. Biodiversity of actinomycetes associated with Caribbean sponges and their potential for natural product discovery. Mar. Biotechnol. (N. Y.) 2013, 15, 413-424.
39. Montalvo, N.F.; Mohamed, N.M.; Enticknap, J.J.; Hill, R.T. Novel actinobacteria from marine sponges. Antonie Van Leeuwenhoek 2005, 87, 29-36. (Pubitemid 40331509)
40. Xin, Y.; Wu, P.; Deng, M.; Zhang, W. Phylogenetic diversity of the culturable rare actinomycetes in marine sponge Hymeniacidon perlevis by improved isolation media. Wei Sheng Wu Xue Bao 2009, 49, 859-866.
41. Abdelmohsen, U.R.; Bayer, K.; Hentschel, U. Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat. Prod. Rep. 2014, 31, 381-399.
42. Webster, N.S.; Wilson, K.J.; Blackall, L.L.; Hill, R.T. Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl. Environ. Microbiol. 2001, 67, 434-444. (Pubitemid 32044447)
43. Mincer, T.J.; Fenical, W.; Jensen, P.R. Culture-dependent and culture-independent diversity within the obligate marine actinomycete genus Salinispora. Appl. Environ. Microbiol. 2005, 71, 7019-7028. (Pubitemid 43194191)
44. Prieto-Davo, A.; Villarreal-Gomez, L.J.; Forschner-Dancause, S.; Bull, A.T.; Stach, J.E.; Smith, D.C.; Rowley, D.C.; Jensen, P.R. Targeted search for actinomycetes from near-shore and deep-sea marine sediments. FEMS Microbiol. Ecol. 2013, 84, 510-518.
45. Asolkar, R.N.; Kirkland, T.N.; Jensen, P.R.; Fenical, W. Arenimycin, an antibiotic effective against rifampin- and methicillin-resistant Staphylococcus aureus from the marine actinomycete Salinispora arenicola. J. Antibiot. (Tokyo) 2010, 63, 37-39.
46. 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. 2012, 14, 270-280.
47. Schneemann, I.; Nagel, K.; Kajahn, I.; Labes, A.; Wiese, J.; Imhoff, J.F. Comprehensive investigation of marine actinobacteria associated with the sponge Halichondria panicea. Appl. Environ. Microbiol. 2010, 76, 3702-3714.
48. Bultel-Ponce, V.V.; Debitus, C.; Berge, J.P.; Cerceau, C.; Guyot, M. Metabolites from the sponge-associated bacterium Micrococcus luteus. J. Mar. Biotechnol. 1998, 6, 233-236. (Pubitemid 29308243)
49. Palomo, S.; Gonzalez, I.; de la Cruz, M.; Martin, J.; Tormo, J.R.; Anderson, M.; Hill, R.T.; Vicente, F.; Reyes, F.; Genilloud, O. Sponge-derived Kocuria and Micrococcus spp. as sources of the new thiazolyl peptide antibiotic kocurin. Mar. Drugs 2013, 11, 1071-1086.
50. Forner, D.; Berrue, F.; Correa, H.; Duncan, K.; Kerr, R.G. Chemical dereplication of marine actinomycetes by liquid chromatography-high resolution mass spectrometry profiling and statistical analysis. Anal. Chim. Acta 2013, 805, 70-79.
51. Chauhan, D.; Catley, L.; Li, G.; Podar, K.; Hideshima, T.; Velankar, M.; Mitsiades, C.; Mitsiades, N.; Yasui, H.; Letai, A.; et al. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell 2005, 8, 407-419.
52. Kim, T.K.; Hewavitharana, A.K.; Shaw, P.N.; Fuerst, J.A. Discovery of a new source of rifamycin antibiotics in marine sponge actinobacteria by phylogenetic prediction. Appl. Environ. Microbiol. 2006, 72, 2118-2125.
53. Jensen, P.R.; Williams, P.G.; Oh, D.C.; Zeigler, L.; Fenical, W. Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl. Environ. Microbiol. 2007, 73, 1146-1152.
54. Williams, P.G.; Asolkar, R.N.; Kondratyuk, T.; Pezzuto, J.M.; Jensen, P.R.; Fenical, W. Saliniketals A and B, bicyclic polyketides from the marine actinomycete Salinispora arenicola. J. Nat. Prod. 2007, 70, 83-88.
55. Oh, D.C.; Gontang, E.A.; Kauffman, C.A.; Jensen, P.R.; Fenical, W. Salinipyrones and pacificanones, mixed-precursor polyketides from the marine actinomycete Salinispora pacifica. J. Nat. Prod. 2008, 71, 570-575. (Pubitemid 351656188)
56. May, F.J.; Davis, C.T.; Tesh, R.B.; Barrett, A.D. Phylogeography of West Nile virus: From the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J. Virol. 2011, 85, 2964-2974.
57. De Filette, M.; Soehle, S.; Ulbert, S.; Richner, J.; Diamond, M.S.; Sinigaglia, A.; Barzon, L.; Roels, S.; Lisziewicz, J.; Lorincz, O.; Sanders, N.N. Vaccination of mice using the West Nile Virus E-Protein in a DNA prime-protein boost strategy stimulates cell-mediated immunity and protects mice against a lethal challenge. PLoS One 2014, 9, e87837.
58. Samanta, S.; Cui, T.; Lam, Y. Discovery, synthesis, and in vitro in vitro evaluation of West Nile virus protease inhibitors based on the 9,10-dihydro-3H,4aH-1,3,9,10a-tetraazaphenanthren-4-one scaffold. ChemMedChem 2012, 7, 1210-1216.
59. Bode, H.B.; Bethe, B.; Hofs, R.; Zeeck, A. Big effects from small changes: Possible ways to explore nature's chemical diversity. ChemBioChem 2002, 3, 619-627. (Pubitemid 36004525)
60. Abdelmohsen, U.R.; Zhang, G.L.; Philippe, A.; Schmitz, W.; Pimentel-Elardo, S.M.; Hertlein-Amslinger, B.; Hentschel, U.; Bringmann, G. Cyclodysidins A-D, cyclic lipopeptides from the marine sponge-derived Streptomyces strain RV15. Tetrahedron Lett. 2012, 53, 23-29.
61. Ashelford, K.E.; Chuzhanova, N.A.; Fry, J.C.; Jones, A.J.; Weightman, A.J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 2005, 71, 7724-7736. (Pubitemid 41803890)
62. Wang, Q.; Garrity, G.M.; Tiedje, J.M.; Cole, J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73, 5261-5267. (Pubitemid 47326658)
63. Pruesse, E.; Peplies, J.; Glockner, F.O. SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 2012, 28, 1823-1829.
64. Capella-Gutierrez, S.; Silla-Martinez, J.M.; Gabaldon, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972-1973.
65. Keane, T.M.; Creevey, C.J.; Pentony, M.M.; Naughton, T.J.; McLnerney, J.O. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 2006, 6, 29.
66. Stamatakis, A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22, 2688-2690. (Pubitemid 44642609)
67. Stover, B.C.; Muller, K.F. TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform. 2010, 11, 7.
68. Ayuso-Sacido, A. Genilloud, O. 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. 2005, 49, 10-24. (Pubitemid 40747800)
69. Ayuso, A.; Clark, D.; Gonzalez, I.; Salazar, O.; Anderson, A.; Genilloud, O. A novel actinomycete strain de-replication approach based on the diversity of polyketide synthase and nonribosomal peptide synthetase biosynthetic pathways. Appl. Microbiol. Biotechnol. 2005, 67, 795-806. (Pubitemid 40905099)
70. 50 in studies of drug resistance of malaria parasites. Acta Trop. 1993, 55, 257-261.
71. Ponte-Sucre, A.; Vicik, R.; Schultheis, M.; Schirmeister, T.; Moll, H. Aziridine-2,3-dicarboxylates, peptidomimetic cysteine protease inhibitors with antileishmanial activity. Antimicrob. Agents Chemother. 2006, 50, 2439-2447. (Pubitemid 43993184)