Species-Specific Secondary Metabolite Production in Marine Actinomycetes of the Genus Salinispora (cid:1)

Here we report associations between secondary metabolite production and phylogenetically distinct but closely related marine actinomycete species belonging to the genus Salinispora . The pattern emerged in a study that included global collection sites, and it indicates that secondary metabolite production can be a species- specific, phenotypic trait associated with broadly distributed bacterial populations. Associations between actinomycete phylotype and chemotype revealed an effective, diversity-based approach to natural product discovery that contradicts the conventional wisdom that secondary metabolite production is strain specific. The structural diversity of the metabolites observed, coupled with gene probing and phylogenetic analyses, impli- cates lateral gene transfer as a source of the biosynthetic genes responsible for compound production. These results conform to a model of selection-driven pathway fixation occurring subsequent to gene acquisition and provide a rare example in which demonstrable physiological traits have been correlated to the fine-scale phylogenetic architecture of an environmental bacterial community.

[1]  H. Zähner What are secondary metabolites? , 2008, Folia Microbiologica.

[2]  J. Davies Are antibiotics naturally antibiotics? , 2006, Journal of Industrial Microbiology and Biotechnology.

[3]  Amitha K. Hewavitharana,et al.  Discovery of a New Source of Rifamycin Antibiotics in Marine Sponge Actinobacteria by Phylogenetic Prediction , 2006, Applied and Environmental Microbiology.

[4]  D. Oh,et al.  Cyanosporasides A and B, chloro- and cyano-cyclopenta[a]indene glycosides from the marine actinomycete "Salinispora pacifica". , 2006, Organic letters.

[5]  Jørn Smedsgaard,et al.  Phenotypic taxonomy and metabolite profiling in microbial drug discovery. , 2005, Natural product reports.

[6]  T. Mincer,et al.  Culturable marine actinomycete diversity from tropical Pacific Ocean sediments. , 2005, Environmental microbiology.

[7]  P. Williams,et al.  Sporolides A and B: structurally unprecedented halogenated macrolides from the marine actinomycete Salinispora tropica. , 2005, Organic letters.

[8]  D. Dubnau,et al.  Structure of the Bacillus subtilis quorum-sensing peptide pheromone ComX , 2005, Nature chemical biology.

[9]  Vincent Daubin,et al.  Examining bacterial species under the specter of gene transfer and exchange , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Garson,et al.  Marine actinomycetes related to the "Salinospora" group from the Great Barrier Reef sponge Pseudoceratina clavata. , 2005, Environmental microbiology.

[11]  H. Floss,et al.  Rifamycin-mode of action, resistance, and biosynthesis. , 2005, Chemical reviews.

[12]  János Bérdy,et al.  Bioactive microbial metabolites. , 2005, The Journal of antibiotics.

[13]  J. Parkhill,et al.  Comparative genomic structure of prokaryotes. , 2004, Annual review of genetics.

[14]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[15]  P. Wiener,et al.  Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters , 2001, Antonie van Leeuwenhoek.

[16]  Gregory L. Challis,et al.  Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Mincer,et al.  Salinosporamide A: a highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus salinospora. , 2003, Angewandte Chemie.

[18]  L. Heide,et al.  Molecular cloning and sequence analysis of the clorobiocin biosynthetic gene cluster: new insights into the biosynthesis of aminocoumarin antibiotics. , 2002, Microbiology.

[19]  William Fenical,et al.  Widespread and Persistent Populations of a Major New Marine Actinomycete Taxon in Ocean Sediments , 2002, Applied and Environmental Microbiology.

[20]  B. Barrell,et al.  Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) , 2002, Nature.

[21]  G. Winkelmann Microbial siderophore-mediated transport. , 2001, Biochemical Society transactions.

[22]  F. Cohan What are bacterial species? , 2002, Annual review of microbiology.

[23]  Yoshiyuki Sakaki,et al.  Genome sequence of an industrial microorganism Streptomyces avermitilis: Deducing the ability of producing secondary metabolites , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Koonin,et al.  Horizontal gene transfer in prokaryotes: quantification and classification. , 2001, Annual review of microbiology.

[25]  R. Firn,et al.  The evolution of secondary metabolism – a unifying model , 2000, Molecular microbiology.

[26]  William Fenical,et al.  Cyclomarins A—C, New Antiinflammatory Cyclic Peptides Produced by a Marine Bacterium (Streptomyces sp.). , 2000 .

[27]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[28]  J. Hacker,et al.  Pathogenicity islands and the evolution of microbes. , 2000, Annual review of microbiology.

[29]  D. Sherman,et al.  Genetic Localization and Molecular Characterization of Two Key Genes (mitAB) Required for Biosynthesis of the Antitumor Antibiotic Mitomycin C , 1999, Journal of bacteriology.

[30]  J. Lake,et al.  Horizontal gene transfer among genomes: the complexity hypothesis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[31]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[32]  J. Lawrence Selfish operons and speciation by gene transfer. , 1997, Trends in microbiology.

[33]  M. Achtman,et al.  A global gene pool in the neisseriae. , 1996, Molecular microbiology.

[34]  S. Ōmura,et al.  Staurosporine, a potentially important gift from a microorganism. , 1995, The Journal of antibiotics.

[35]  P. Jensen,et al.  Distribution of actinomycetes in near-shore tropical marine sediments , 1991, Applied and environmental microbiology.

[36]  H. Kinashi,et al.  Giant linear plasmids in Streptomyces which code for antibiotic biosynthesis genes , 1987, Nature.

[37]  S. Waksman,et al.  Strain Specificity and Production of Antibiotic Substances. , 1943, Proceedings of the National Academy of Sciences of the United States of America.