Polyketide synthase gene diversity within the microbiome of the sponge Arenosclera brasiliensis, endemic to the southern Atlantic Ocean

Applied and Environmental Microbiology

Volumn 79, Issue 5, 2013, Pages 1598-1605

  Trindade Silva, Amaro E ^a,b   Rua, Cintia P J ^b   Andrade, Bruno G N ^c   Vicente, Ana Carolina Paulo ^c   Silva, Genivaldo G Z ^d   Berlinck, Roberto G S ^a   Thompson, Fabiano L ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d San Diego State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLICONS; ANTI-BACTERIAL ACTIVITY; ATLANTIC OCEAN; CONTIGS; CYTOTOXIC; HIGH-THROUGHPUT SEQUENCING; KETOSYNTHASE; MARINE SPONGE; METAGENOMES; MICROBIOME; MICROBIOTAS; PHYLOGENETIC ANALYSIS; PHYLOGENETIC RECONSTRUCTION; POLYKETIDE SYNTHASE GENES; POLYKETIDE SYNTHASES; POLYKETIDES; SECONDARY METABOLITES;

BACTERIA; METABOLITES; PLANTS (BOTANY);

GENES;

POLYKETIDE SYNTHASE;

BIOME; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENETIC VARIATION; GENOME; MARINE ECOSYSTEM; METABOLITE; MICROBIAL COMMUNITY; PHYLOGENETICS; SPONGE; SYNTHETIC APERTURE RADAR;

ANIMAL; ARTICLE; ATLANTIC OCEAN; GENETIC VARIABILITY; GENETICS; HIGH THROUGHPUT SEQUENCING; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SPONGE (PORIFERA);

ANIMALS; ATLANTIC OCEAN; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METAGENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYKETIDE SYNTHASES; PORIFERA;

ATLANTIC OCEAN; ATLANTIC OCEAN (SOUTH);

EID: 84874717421     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03354-12     Document Type: Article

References (52)

1. Vacelet J, Donadey C. 1977. Electron microscope study of the association between some sponges and bacteria. J. Exp. Marine Biol. Ecol. 30:301-314.
2. Taylor MW, Radax R, Steger D, Wagner M. 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71:295-347.
3. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster N, Hentschel U, Taylor MW. 2011. Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J. 6:564- 576.
4. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW. 2012. Sponge-specific clusters revisited: a comprehensive phylogeny of spongeassociated microorganisms. Environ. Microbiol. 14:517-524.
5. Webster NS, Taylor MW, Behnam F, Lucker S, Rattei T, Whalan S, Horn M, Wagner M. 2010. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ. Microbiol. 12:2070-2082.
6. Schmitt S, Hentschel U, Taylor MW. 2011. Deep sequencing reveals diversity and community structure of complex microbiota in five Mediterranean sponges. Hydrobiologia 687:341-351.
7. Pawlik JR. 2011. The chemical ecology of sponges on Caribbean reefs: natural products shape natural systems. Bioscience 61:888-898.
8. Amoutzias GD, Van de Peer Y, Mossialos D. 2008. Evolution and taxonomic distribution of nonribosomal peptide and polyketide synthases. Future Microbiol. 3:361-370.
9. Schmidt EW. 2008. Trading molecules and tracking targets in symbiotic interactions. Nat. Chem. Biol. 4:466-473.
10. de Oliveira JHHL, Nascimento AM, Kossuga MH, Cavalcanti BC, Pessoa CO, Moraes MO, Macedo ML, Ferreira AG, Hajdu E, Pinheiro US, Berlinck RG. 2007. Cytotoxic alkylpiperidine alkaloids from the Brazilian marine sponge Pachychalina alcaloidifera. J. Nat. Prod. 70:538 -543.
11. Ang KKH, Holmes MJ, Higa T, Hamann MT, Kara UA. 2000. In vivo antimalarial activity of the beta-carboline alkaloid manzamine A. Antimicrob. Agents Chemother. 44:1645-1649.
12. Hill RT, Peraud O, Hamann MT, Kamke J. November 2005. Manzamine-producing actinomycetes. US patent 20050244938A1.
13. Fontana A. 2006. Biogenetic proposals and biosynthetic studies on secondary metabolites of opisthobranch molluscs, p 304-332. In Cimino G, Gavagnin M (ed), Molluscs: from chemo-ecological study to biotechnological application. Springer-Verlag, Berlin, Germany.
14. Almeida AM, Hajdu E, Berlinck RGS. 1997. Alcalóides alquilpiridínicos de esponjas marinhas. Quím. Nova 20:170-185.
15. Andersen RJ, van Soest RWM, Kong F. 1996. 3-Alkylpyridine alkaloids isolated from marine sponges in the order Haposclerida, p 301-355. In Pelletier SW (ed), Alkaloids: chemical and biological perspectives, vol 10. Pergamon, London, United Kingdom.
16. Fischbach MA, Walsh CT. 2006. Assembly-line enzymology for polyketide and nonribosomal peptide antibiotics: logic, machinery, and mechanisms. Chem. Rev. 106:3468 -3496.
17. Piel J. 2010. Biosynthesis of polyketides by trans-AT polyketide synthases. Nat. Prod. Rep. 27:996 -1047.
18. Jenke-Kodama H, Borner T, Dittmann E. 2006. Natural biocombinatorics in the polyketide synthase genes of the actinobacterium Streptomyces avermitilis. PLoS Comput. Biol. 2:1210 -1218. doi:10.1371/journal.pcbi.0020132.
19. Nguyen T, Ishida K, Jenke-Kodama H, Dittmann E, Gurgui C, Hochmuth T, Taudien S, Platzer M, Hertweck C, Piel J. 2008. Exploiting the mosaic structure of trans-acyltransferase polyketide synthases for natural product discovery and pathway dissection. Nat. Biotechnol. 26:225- 233.
20. Schirmer A, Gadkari R, Reeves CD, Ibrahim F, DeLong EF, Hutchinson CR. 2005. Metagenomic analysis reveals diverse polyketide synthase gene clusters in microorganisms associated with the marine sponge Discodermia dissoluta. Appl. Environ. Microbiol. 71:4840-4849.
21. Kim TK, Fuerst JA. 2006. Diversity of polyketide synthase genes from bacteria associated with the marine sponge Pseudoceratina clavata: culture-dependent and culture-independent approaches. Environ. Microbiol. 8:1460-1470.
22. Kennedy J, Baker P, Piper C, Cotter PD, Walsh M, Mooij MJ, Bourke MB, Rea MC, O'Connor PM, Ross RP, Hill C, O'Gara F, Marchesi JR, Dobson AD. 2008. Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar. Biotechnol. 11:384-396.
23. Fieseler L, Hentschel U, Grozdanov L, Schirmer A, Wen G, Platzer M, Hrvatin S, Butzke D, Zimmermann K, Piel J. 2007. Widespread occurrence and genomic context of unusually small polyketide synthase genes in microbial consortia associated with marine sponges. Appl. Environ. Microbiol. 73:2144-2155.
24. Fisch KM, Gurgui C, Heycke N, van der Sar SA, Anderson SA, Webb VL, Taudien S, Platzer M, Rubio BK, Robinson SJ, Crews P, Piel J. 2009. Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting. Nat. Chem. Biol. 5:494 -501.
25. O'Halloran JA, Barbosa TM, Morrissey JP, Kennedy J, O'Gara F, Dobson AD. 2011. Diversity and antimicrobial activity of Pseudovibrio spp. from Irish marine sponges. J. Appl. Microbiol. 110:1495-1508.
26. Hochmuth T, Niederkruger H, Gernert C, Siegl A, Taudien S, Platzer M, Crews P, Hentschel U, Piel J. 2010. Linking chemical and microbial diversity in marine sponges: possible role for poribacteria as producers of methyl-branched fatty acids. Chembiochem 11:2572-2578.
27. Torres YR, Berlinck RGS, Magalhaes A, Schefer AB, Ferreira AG, Hajdu E, Muricy G. 2000. Arenosclerins A-C and haliclonacyclamine E, new tetracyclic alkaloids from a Brazilian endemic haplosclerid sponge Arenosclera brasiliensis. J. Nat. Prod. 63:1098 -1105.
28. Torres YR, Berlinck RGS, Nascimento GGF, Fortier SC, Pessoa C, de Moraes MO. 2002. Antibacterial activity against resistant bacteria and cytotoxicity of four alkaloid toxins isolated from the marine sponge Arenosclera brasiliensis. Toxicon 40:885-891.
29. Trindade-Silva AE, Rua C, Silva GG, Dutilh BE, Moreira AP, Edwards RA, Hajdu E, Lobo-Hajdu G, Vasconcelos AT, Berlinck RG, Thompson FL. 2012. Taxonomic and functional microbial signatures of the endemic marine sponge Arenosclera brasiliensis. PLoS One 7:e39905. doi:10.1371 /journal.pone.0039905.
30. Piel J, Hui DQ, Fusetani N, Matsunaga S. 2004. Targeting modular polyketide synthases with iteratively acting acyltransferases from metagenomes of uncultured bacterial consortia. Environ. Microbiol. 6:921-927.
31. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
32. UniProt Consortium. 2012. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40:D71-D75.
33. 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.
34. Eddy SR. 1998. Profile hidden Markov models. Bioinformatics Rev. 14: 755-763.
35. Olson S. 2002. EMBOSS opens up sequence analysis. European Molecular Biology Open Software Suite. Brief. Bioinformatics 3:87-91.
36. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386.
37. Kroken S, Glass L, Taylor JW, Yoder OC, Turgeon BG. 2003. Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc. Natl. Acad. Sci. U. S. A. 100:15670 -15675.
38. Zhang Y, Hurlbert J, White SW, Rock CO. 2006. Roles of the active site water, histidine 303, and phenylalanine 396 in the catalytic mechanism of the elongation condensing enzyme of Streptococcus pneumoniae. J. Biol. Chem. 281:17390 -17399.
39. Qiu X, Choudhry AE, Janson CA, Grooms M, Daines RA, Lonsdale JT, Khandekar SS. 2005. Crystal structure and substrate specificity of the β-ketoacyl-acyl carrier protein synthase III (FabH) from Staphylococcus aureus. Protein Sci. 14:2087-2094.
40. Beyer S, Kunze B, Silakowski B, Müller R. 1999. Metabolic diversity in myxobacteria: identification of the myxalamid and the stigmatellin biosynthetic gene cluster of Stigmatella aurantiaca Sg a15 and a combined polyketide-(poly)peptide gene cluster from the epothilone producing strain Sorangium cellulosum So ce90. Biochim. Biophys. Acta 1445:185-195.
41. Piel J. 2002. A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of Paederus beetles. Proc. Natl. Acad. Sci. U. S. A. 99:14002-14007.
42. Siegl A, Hentschel U. 2010. PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ. Microbiol. 2:507-513.
43. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T, Hentschel U. 2011. Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J. 5:61-70.
44. Nett M, Ikeda H, Moore BS. 2009. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep. 26:1362- 1384.
45. Metz JG. 2001. Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293:290 -293.
46. Ahlert J. 2002. The calicheamicin gene cluster and its iterative type I enediyne PKS. Science 297:1173-1176.
47. Campbell EL, Cohen MF, Meeks JC. 1997. A polyketide-synthase-like gene is involved in the synthesis of heterocyst glycolipids in Nostoc punctiforme strain ATCC 29133. Arch. Microbiol. 167:251-258.
48. Huntley S, Zhang Y, Treuner-Lange A, Kneip S, Sensen CW, Søgaard-Andersen L. 2012. Complete genome sequence of the fruiting myxobacterium Corallococcus coralloides DSM 2259. J. Bacteriol. 194:3012-3013.
49. Parada M, Vinardell JM, Ollero FJ, Hidalgo A, Gutierrez R, Buendía-Clavería AM, Lei W, Margaret I, López-Baena FJ, Gil-Serrano AM, Rodríguez-Carvajal MA, Moreno J, Ruiz-Sainz JE. 2006. Sinorhizobium fredii HH103 mutants affected in capsular polysaccharide (KPS) are impaired for nodulation with soybean and Cajanus cajan. Mol. Plant Microbe Interact. 19:43-52.
50. DeShazer D, Waag DM, Fritz DL, Woods DE. 2001. Identification of a Burkholderia mallei polysaccharide gene cluster by subtractive hybridization and demonstration that the encoded capsule is an essential virulence determinant. Microb. Pathog. 30:253-269.
51. Wilkinson CR, Garrone R, Vacelet J. 1984. Marine sponges discriminate between food bacteria and bacterial symbionts: electron microscope radioautography and in situ evidence. Proc. R. Soc. B Biol. Sci. 220:519 -528.
52. Partida-Martinez LP, Hertweck C. 2007. A gene cluster encoding rhizoxin biosynthesis in "Burkholderia rhizoxina", the bacterial endosymbiont of the fungus Rhizopus microsporus. Chembiochem 8:41-45.