Polyketide synthases of bacterial symbionts in sponges - Evolution-based applications in natural products research

Phytochemistry

Volumn 70, Issue 15-16, 2009, Pages 1841-1849

  Hochmuth, Thomas ^a   Piel, Jörn ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Fatty acids; Polyketide synthases; Polyketides; Sponges; Symbiosis; Uncultivated bacteria

Indexed keywords

BIOLOGICAL PRODUCT; POLYKETIDE SYNTHASE;

ANIMAL; BACTERIUM; ENZYMOLOGY; EVOLUTION; GENETICS; MICROBIOLOGY; REVIEW; SPONGE (PORIFERA); SYMBIOSIS;

ANIMALS; BACTERIA; BIOLOGICAL PRODUCTS; EVOLUTION; POLYKETIDE SYNTHASES; PORIFERA; SYMBIOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 70350736731     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2009.04.010     Document Type: Review

References (69)

1. Albertini A.M., Caramori T., Scoffone F., Scotti C., and Galizzi A. Sequence around the 159 region of the Bacillus subtilis genome - the pksX locus spans 33.6 Kb. Microbiology 141 (1995) 299-309
2. Barnathan G., Genin E., Velosaotsy N.E., Kornprobst J.M., Al-Lihaibi S., Al-Sofyani A., and Nongonierma R. Phospholipid fatty acids and sterols of two Cinachyrella sponges from the Saudi Arabian Red Sea: comparison with Cinachyrella species from other origins. Comp. Biochem. Physiol. Part B: Biochem. Mol. Biol. 135 (2003) 297-308
3. Blunt J.W., Copp B.R., Hu W.P., Munro M.H.G., Northcote P.T., and Prinsep M.R. Marine natural products. Nat. Prod. Rep. 26 (2009) 170-244
4. Bode H.B., Ring M.W., Schwar G., Kroppenstedt R.M., Kaiser D., and Müller R. 3-Hydroxy-3-methylglutaryl-coenzyme A (CoA) synthase is involved in biosynthesis of isovaleryl-CoA in the myxobacterium Myxococcus xanthus during fruiting body formation. J. Bacteriol. 188 (2006) 6524-6528
5. Brink D.E., Vance I., and White D.C. Detection of Desulfobacter in oil field environments by non-radioactive DNA probes. Appl. Microbiol. Biotechnol. 42 (1994) 469-475
6. Bumpus S.B., Magarvey N.A., Kelleher N.L., Walsh C.T., and Calderone C.T. Polyunsaturated fatty-acid-like trans-enoyl reductases utilized in polyketide biosynthesis. J. Am. Chem. Soc. 130 (2008) 11614
7. Calderone C.T., Kowtoniuk W.E., Kelleher N.L., Walsh C.T., and Dorrestein P.C. Convergence of isoprene and polyketide biosynthetic machinery: isoprenyl-S-carrier proteins in the pksX pathway of Bacillus subtilis. Proc. Natl. Acad. Sci. USA 103 (2006) 8977-8982
8. Carballeira N., Thompson J.E., Ayanoglu E., and Djerassi C. Biosynthetic studies of marine lipids. 5. The biosynthesis of long-chain branched fatty acids in marine sponges. J. Org. Chem. 51 (1986) 2751-2756
9. Carballeira N.M., Sostre A., Stefanov K., Popov S., Kujumgiev A., Dimitrova-Konaklieva S., Tosteson C.G., and Tosteson T.R. The fatty acid composition of a Vibrio alginolyticus associated with the alga Cladophora coelothrix. Identification of the 9-methyl-10-hexadecenoic acid. Lipids 32 (1997) 1271-1275
10. Carballeira N.M., Miranda C., Lozano C.M., Nechev J.T., Ivanova A., Ilieva M., Tzvetkova I., and Stefanov K. Characterization of methyl-branched chain fatty acids from a halophilic Bacillus species. J. Nat. Prod. 64 (2001) 256-259
11. Carballeira N.M., Oyola D., Vicente J., and Rodriguez A.D. Identification of alpha-methoxylated phospholipid fatty acids in the Caribbean sponge Erylus goffrilleri. Lipids 42 (2007) 1047-1053
12. Castoe T.A., Stephens T., Noonan B.P., and Calestani C. A group of type I polyketide synthases (PKS) in animals and the complex phylogenomics of PKSs. Gene 392 (2007) 47-58
13. Chen X.H., Vater J., Piel J., Franke P., Scholz R., Schneider K., Koumoutsi A., Hitzeroth G., Grammel N., Strittmatter A.W., Gottschalk G., Süßmuth R.D., and Borriss R. Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J. Bacteriol. 188 (2006) 4024-4036
14. Cheng Y.Q., Tang G.L., and Shen B. Type I polyketide synthase requiring a discrete acyltransferase for polyketide biosynthesis. Proc. Natl. Acad. Sci. USA 100 (2003) 3149-3154
15. Chou S., Chedore P., Haddad A., Paul N.R., and Kasatiya S. Direct identification of Mycobacterium species in Bactec 7H12B medium by gas-liquid chromatography. J. Clin. Microbiol. 34 (1996) 1317-1320
16. Edwards D.J., Marquez B.L., Nogle L.M., McPhail K., Goeger D.E., Roberts M.A., and Gerwick W.H. Structure and biosynthesis of the jamaicamides, mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem. Biol. 11 (2004) 817-833
17. El-Sayed A.K., Hothersall J., Cooper S.M., Stephens E., Simpson T.J., and Thomas C.M. Characterization of the mupirocin biosynthesis gene cluster from Pseudomonas fluorescens NCIMB 10586. Chem. Biol. 10 (2003) 419-430
18. Embley T.M., Wait R., Dobson G., and Goodfellow M. Fatty acid composition in the classification of Saccharopolyspora hirsuta. FEMS Microbiol. Lett. 41 (1987) 131-135
19. Faulkner D.J., He H.Y., Unson M.D., Bewley C.A., and Garson M.J. Metabolites from marine sponges - are symbionts important. Gazz. Chim. Ital. 123 (1993) 301-307
20. Fieseler L., Horn M., Wagner M., and Hentschel U. Discovery of the candidate phylum "Poribacteria" in marine sponges. Appl. Environ. Microbiol. 70 (2004) 3724-3732
21. Fieseler L., Hentschel U., Grozdanov L., Schirmer A., Wen G., Platzer M., Hrvatin S., Butzke D., Zimmermann K., and Piel J. Widespread occurrence and genomic context of unusually small polyketide synthase genes in microbial consortia associated with marine sponges. Appl. Environ. Microbiol. 73 (2007) 2144-2155
22. Fischbach M.A., and Walsh C.T. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106 (2006) 3468-3496
23. Fujii I. Heterologous expression systems for polyketide synthases. Nat. Prod. Rep. 26 (2009) 155-169
24. Gillan F.T., Stoilov I.L., Thompson J.E., Hogg R.W., Wilkinson C.R., and Djerassi C. Phospholipid studies of marine organisms. 21. Fatty acids as biological markers for bacterial symbionts in sponges. Lipids 23 (1988) 1139-1145
25. Gu L.C., Jia J.Y., Liu H.C., Hakansson K., Gerwick W.H., and Sherman D.H. Metabolic coupling of dehydration and decarboxylation in the curacin A pathway: functional identification of a mechanistically diverse enzyme pair. J. Am. Chem. Soc. 128 (2006) 9014-9015
26. Hentschel U., Usher K.M., and Taylor M.W. Marine sponges as microbial fermenters. FEMS Microbiol. Ecol. 55 (2006) 167-177
27. Hrvatin S., and Piel J. Rapid isolation of rare clones from highly complex DNA libraries by PCR analysis of liquid gel pools. J. Microbiol. Meth. 68 (2007) 434-436
28. Jackson M., Stadthagen G., and Gicquel B. Long-chain multiple methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis: biosynthesis, transport, regulation and biological activities. Tuberculosis (Edinb.) 87 (2007) 78-86
29. Jenke-Kodama H., Sandmann A., Müller R., and Dittmann E. Evolutionary implications of bacterial polyketide synthases. Mol. Biol. Evol. 22 (2005) 2027-2039
30. Jenke-Kodama H., Borner T., and Dittmann E. Natural biocombinatorics in the polyketide synthase genes of the actinobacterium Streptomyces avermitilis. PLoS Comput. Biol. 2 (2006) e132
31. Kaneda T. Iso-fatty and anteiso-fatty acids in bacteria - biosynthesis, function, and taxonomic significance. Microbiol. Rev. 55 (1991) 288-302
32. Kim T.K., and Fuerst J.A. Diversity of polyketide synthase genes from bacteria associated with the marine sponge Pseudoceratina clavata: culture-dependent and culture-independent approaches. Environ. Microbiol. 8 (2006) 1460-1470
33. Kumar M., Verma M., and Lal R. Devosia chinhatensis sp. Nov., isolated from a hexachlorocyclohexane (HCH) dump site in India. Int. J. Syst. Evol. Microbiol. 58 (2008) 861-865
34. Leibundgut M., Maier T., Jenni S., and Ban N. The multienzyme architecture of eukaryotic fatty acid synthases. Curr. Opin. Struct. Biol. 18 (2008) 714-725
35. Lipski A., Spieck E., Makolla A., and Altendorf K. Fatty acid profiles of nitrite-oxidizing bacteria reflect their phylogenetic heterogeneity. Syst. Appl. Microbiol. 24 (2001) 377-384
36. Love G.D., Grosjean E., Stalvies C., Fike D.A., Grotzinger J.P., Bradley A.S., Kelly A.E., Bhatia M., Meredith W., Snape C.E., Bowring S.A., Condon D.J., and Summons R.E. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457 (2009) U715-U718
37. Maier T., Leibundgut M., and Ban N. The crystal structure of a mammalian fatty acid synthase. Science 321 (2008) 1315-1322
38. Matsunaga S., Fusetani N., and Nakao Y. Eight cytotoxic metabolites closely related to onnamide A from 2 marine sponges of the genus Theonella. Tetrahedron 48 (1992) 8369-8376
39. Moldenhauer J., Chen X., Borriss R., and Piel J. Biosynthesis of the antibiotic bacillaene, the product of a giant polyketide synthase complex of the trans-AT family. Angew. Chem. Int. Ed. 46 (2007) 8195-8197
40. Nechev J., Christie W.W., Robaina R., de Diego F., Popov S., and Stefanov K. Chemical composition of the sponge Hymeniacidon sanguinea from the Canary Islands. Comp. Biochem. Physiol. Part A: Mol. Integr. Physiol. 137 (2004) 365-374
41. Nguyen T., Ishida K., Jenke-Kodama H., Dittmann E., Gurgui C., Hochmuth T., Taudien S., Platzer M., Hertweck C., and Piel J. Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection. Nat. Biotechnol. 26 (2008) 225-233
42. Pape, T., 2004. Lipidbiomarker Schwammassoziierter Bakterien und Archaeen. Instititut für Geowissenschaften. PhD Thesis. University of Hamburg, Hamburg, p. 164.
43. Parada M., Vinardell J.M., Ollero F.J., Hidalgo A., Gutierrez R., Buendia-Claveria A.M., Lei W., Margaret I., Lopez-Baena F.J., Gil-Serrano A.M., Rodriguez-Carvajal M.A., Moreno J., and Ruiz-Sainz J.E. Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol. Plant Microbe Interact. 19 (2006) 43-52
44. Partida-Martinez L.P., and Hertweck C. Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437 (2005) 884-888
45. Partida-Martinez L.P., and Hertweck C. A gene cluster encoding rhizoxin biosynthesis in "Burkholderia rhizoxina", the bacterial endosymbiont of the fungus Rhizopus microsporus. ChemBioChem. 8 (2007) 41-45
46. Paul V.J., and Ritson-Williams R. Marine chemical ecology. Nat. Prod. Rep. 25 (2008) 662-695
47. Pawlik J.R. Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Mar. Biol. 30 (1992) 273-335
48. Piel J. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. USA 99 (2002) 14002-14007
49. Piel J. Metabolites from symbiotic bacteria. Nat. Prod. Rep. 21 (2004) 519-538
50. Piel J. Bacterial symbionts: prospects for the sustainable production of invertebrate-derived pharmaceuticals. Curr. Med. Chem. 13 (2006) 39-50
51. Piel J., Hui D., Fusetani N., and Matsunaga S. Targeting modular polyketide synthases with iteratively acting acyltransferases from metagenomes of uncultured bacterial consortia. Environ. Microbiol. 6 (2004) 921-927
52. Piel J., Hui D., Wen G., Butzke D., Platzer M., Fusetani N., and Matsunaga S. Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc. Natl. Acad. Sci. USA 101 (2004) 16222-16227
53. Piel J., Wen G., Platzer M., and Hui D. Unprecedented diversity of catalytic domains in the first four modules of the putative pederin polyketide synthase. ChemBioChem. 5 (2004) 93-98
54. Pond J.L., Langworthy T.A., and Holzer G. Long-chain diols: a class of membrane lipids from a thermophilic bacterium. Science 231 (1986) 1134-1136
55. Pulsawat N., Kitani S., and Nihira T. Characterization of biosynthetic gene cluster for the production of virginiamycin M, a streptogramin type A antibiotic, in Streptomyces virginiae. Gene 393 (2007) 31-42
56. Radmacher E., Alderwick L.J., Besra G.S., Brown A.K., Gibson K.J., Sahm H., and Eggeling L. Two functional FAS-I type fatty acid synthases in Corynebacterium glutamicum. Microbiology 151 (2005) 2421-2427
57. Ridley C.P., Lee H.Y., and Khosla C. Evolution of polyketide synthases in bacteria. Proc. Natl. Acad. Sci. USA 105 (2008) 4595-4600
58. Rod'kina S.A. Fatty acids and other lipids of sponges. Russ. J. Mar. Biol. 31 (2005) S49-S60
59. Salomon C.E., Magarvey N.A., and Sherman D.H. Merging the potential of microbial genetics with biological and chemical diversity: an even brighter future for marine natural product drug discovery. Nat. Prod. Rep. 21 (2004) 105-121
60. Santavy D.L., Willenz P., and Colwell R.R. Phenotypic study of bacteria associated with the caribbean sclerosponge, Ceratoporella nicholsoni. Appl. Environ. Microbiol. 56 (1990) 1750-1762
61. Schirmer A., Gadkari R., Reeves C.D., Ibrahim F., DeLong E.F., and Hutchinson C.R. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl. Environ. Microbiol. 71 (2005) 4840-4849
62. Schmidt E.W. Trading molecules and tracking targets in symbiotic interactions. Nat. Chem. Biol. 4 (2008) 466-473
63. Simunovic V., and Müller R. 3-Hydroxy-3-methylglutaryl-CoA-like synthases direct the formation of methyl and ethyl side groups in the biosynthesis of the antibiotic myxovirescin A. ChemBioChem. 8 (2007) 497-500
64. Smith S., and Tsai S.C. The type I fatty acid and polyketide synthases: a tale of two megasynthases. Nat. Prod. Rep. 24 (2007) 1041-1072
65. Sudek S., Lopanik N.B., Waggoner L.E., Hildebrand M., Anderson C., Liu H., Patel A., Sherman D.H., and Haygood M.G. Identification of the putative bryostatin polyketide synthase gene cluster from "Candidatus endobugula sertula", the uncultivated microbial symbiont of the marine bryozoan Bugula neritina. J. Nat. Prod. 70 (2007) 67-74
66. Taylor M.W., Radax R., Steger D., and Wagner M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71 (2007) 295-347
67. Thiel V., Jenisch A., Wörheide G., Löwenberg A., Reitner J., and Michaelis W. Mid-chain branched alkanoic acids from "living fossil" demosponges: a link to ancient sedimentary lipids?. Org. Geochem. 30 (1999) 1-14
68. Vacelet J., and Donadey C. Electron-microscope study of association between some sponges and bacteria. J. Exp. Mar. Biol. Ecol. 30 (1977) 301-314
69. Weissman K.J., and Müller R. Protein-protein interactions in multienzyme megasynthetases. ChemBioChem. 9 (2008) 826-848