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Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula.

ABSTRACT: Filamentous cyanobacteria of the genus Lyngbya are important contributors to coral reef ecosystems, occasionally forming dominant cover and impacting the health of many other co-occurring organisms. Moreover, they are extraordinarily rich sources of bioactive secondary metabolites, with 35% of all reported cyanobacterial natural products deriving from this single pantropical genus. However, the true natural product potential and life strategies of Lyngbya strains are poorly understood because of phylogenetic ambiguity, lack of genomic information, and their close associations with heterotrophic bacteria and other cyanobacteria. To gauge the natural product potential of Lyngbya and gain insights into potential microbial interactions, we sequenced the genome of Lyngbya majuscula 3L, a Caribbean strain that produces the tubulin polymerization inhibitor curacin A and the molluscicide barbamide, using a combination of Sanger and 454 sequencing approaches. Whereas ? 293,000 nucleotides of the draft genome are putatively dedicated to secondary metabolism, this is far too few to encode a large suite of Lyngbya metabolites, suggesting Lyngbya metabolites are strain specific and may be useful in species delineation. Our analysis revealed a complex gene regulatory network, including a large number of sigma factors and other regulatory proteins, indicating an enhanced ability for environmental adaptation or microbial associations. Although Lyngbya species are reported to fix nitrogen, nitrogenase genes were not found in the genome or by PCR of genomic DNA. Subsequent growth experiments confirmed that L. majuscula 3L is unable to fix atmospheric nitrogen. These unanticipated life history characteristics challenge current views of the genus Lyngbya.

SUBMITTER: Jones AC

PROVIDER: S-EPMC3102346 | biostudies-literature | 2011 May

REPOSITORIES: biostudies-literature

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Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula.

Jones Adam C AC Monroe Emily A EA Podell Sheila S Hess Wolfgang R WR Klages Sven S Esquenazi Eduardo E Niessen Sherry S Hoover Heather H Rothmann Michael M Lasken Roger S RS Yates John R JR Reinhardt Richard R Kube Michael M Burkart Michael D MD Allen Eric E EE Dorrestein Pieter C PC Gerwick William H WH Gerwick Lena L

Proceedings of the National Academy of Sciences of the United States of America 20110509 21

Filamentous cyanobacteria of the genus Lyngbya are important contributors to coral reef ecosystems, occasionally forming dominant cover and impacting the health of many other co-occurring organisms. Moreover, they are extraordinarily rich sources of bioactive secondary metabolites, with 35% of all reported cyanobacterial natural products deriving from this single pantropical genus. However, the true natural product potential and life strategies of Lyngbya strains are poorly understood because of ...[more]

PMID: 21555588

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Project description:The marine cyanobacterium Lyngbya majuscula is a prolific producer of bioactive secondary metabolites. Although biosynthetic gene clusters encoding several of these compounds have been identified, little is known about how these clusters of genes are transcribed or regulated, and techniques targeting genetic manipulation in Lyngbya strains have not yet been developed. We conducted transcriptional analyses of the jamaicamide gene cluster from a Jamaican strain of Lyngbya majuscula, and isolated proteins that could be involved in jamaicamide regulation.An unusually long untranslated leader region of approximately 840 bp is located between the jamaicamide transcription start site (TSS) and gene cluster start codon. All of the intergenic regions between the pathway ORFs were transcribed into RNA in RT-PCR experiments; however, a promoter prediction program indicated the possible presence of promoters in multiple intergenic regions. Because the functionality of these promoters could not be verified in vivo, we used a reporter gene assay in E. coli to show that several of these intergenic regions, as well as the primary promoter preceding the TSS, are capable of driving beta-galactosidase production. A protein pulldown assay was also used to isolate proteins that may regulate the jamaicamide pathway. Pulldown experiments using the intergenic region upstream of jamA as a DNA probe isolated two proteins that were identified by LC-MS/MS. By BLAST analysis, one of these had close sequence identity to a regulatory protein in another cyanobacterial species. Protein comparisons suggest a possible correlation between secondary metabolism regulation and light dependent complementary chromatic adaptation. Electromobility shift assays were used to evaluate binding of the recombinant proteins to the jamaicamide promoter region.Insights into natural product regulation in cyanobacteria are of significant value to drug discovery and biotechnology. To our knowledge, this is the first attempt to characterize the transcription and regulation of secondary metabolism in a marine cyanobacterium. If jamaicamide is light regulated, this mechanism would be similar to other cyanobacterial natural product gene clusters such as microcystin LR. These findings could aid in understanding and potentially assisting the management of toxin production by Lyngbya in the environment.

Dataset Information

Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula.

Publications

Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula.

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