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Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters.

ABSTRACT: Traditional natural product discovery methods have nearly exhausted the accessible diversity of microbial chemicals, making new sources and techniques paramount in the search for new molecules. Marine actinomycete bacteria have recently come into the spotlight as fruitful producers of structurally diverse secondary metabolites, and remain relatively untapped. In this study, we sequenced 21 marine-derived actinomycete strains, rarely studied for their secondary metabolite potential and under-represented in current genomic databases. We found that genome size and phylogeny were good predictors of biosynthetic gene cluster diversity, with larger genomes rivalling the well-known marine producers in the Streptomyces and Salinispora genera. Genomes in the Micrococcineae suborder, however, had consistently the lowest number of biosynthetic gene clusters. By networking individual gene clusters into gene cluster families, we were able to computationally estimate the degree of novelty each genus contributed to the current sequence databases. Based on the similarity measures between all actinobacteria in the Joint Genome Institute's Atlas of Biosynthetic gene Clusters database, rare marine genera show a high degree of novelty and diversity, with Corynebacterium, Gordonia, Nocardiopsis, Saccharomonospora and Pseudonocardia genera representing the highest gene cluster diversity. This research validates that rare marine actinomycetes are important candidates for exploration, as they are relatively unstudied, and their relatives are historically rich in secondary metabolites.

SUBMITTER: Schorn MA

PROVIDER: S-EPMC5756490 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters.

Schorn Michelle A MA Alanjary Mohammad M MM Aguinaldo Kristen K Korobeynikov Anton A Podell Sheila S Patin Nastassia N Lincecum Tommie T Jensen Paul R PR Ziemert Nadine N Moore Bradley S BS

Microbiology (Reading, England) 20161027 12

Traditional natural product discovery methods have nearly exhausted the accessible diversity of microbial chemicals, making new sources and techniques paramount in the search for new molecules. Marine actinomycete bacteria have recently come into the spotlight as fruitful producers of structurally diverse secondary metabolites, and remain relatively untapped. In this study, we sequenced 21 marine-derived actinomycete strains, rarely studied for their secondary metabolite potential and under-repr ...[more]

PMID: 27902408

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Project description:Marine actinomycetes are an important source of antibiotics, but many of them are yet to be explored in terms of taxonomy, ecology, and functional activity. In this study, two marine actinobacterial strains, designated SCSIO 64649T and SCSIO 03032, were isolated, and the potential for bioactive natural product discovery was evaluated based on genome mining, compound detection, and antimicrobial activity. Phylogenetic analysis of the 16S rRNA gene sequences showed that strain SCSIO 64649T formed a single clade with SCSIO 03032 (similarity 99.5%) and sister clades with the species Streptomyces specialis DSM 41924T (97.1%) and Streptomyces manganisoli MK44T (96.8%). The whole genome size of strain SCSIO 64649T was 6.63 Mbp with a 73.6% G + C content. The average nucleotide identity and digital DNA-DNA hybridization between strain SCSIO 64649T and its closest related species were well below the thresholds recommended for species delineation. Therefore, according to the results of polyphasic taxonomy analysis, the strains SCSIO 64649T and SCSIO 03032 are proposed to represent a novel species named Streptomyces marincola sp. nov. Furthermore, strains SCSIO 64649T and 03032 encode 37 putative biosynthetic gene clusters, and in silico analysis revealed that this new species has a high potential to produce unique natural products, such as a novel polyene polyketide compounds, two mayamycin analogs, and a series of post-translationally modified peptides. In addition, other important bioactive natural products, such as heronamide F, piericidin A1, and spiroindimicin A, were also detected in strain SCSIO 64649T. Finally, this new species' metabolic crude extract showed a strong antimicrobial activity. Thanks to the integration of all these analyses, this study demonstrates that the novel species Streptomyces marincola has a unique and novel secondary metabolite biosynthetic potential that not only is beneficial to possible marine hosts but that could also be exploited for industrial applications.

Project description:BackgroundBiosynthetic gene clusters produce a wide range of metabolites with activities that are of interest to the pharmaceutical industry. Specific interest is shown towards those metabolites that exhibit antimicrobial activities against multidrug-resistant bacteria that have become a global health threat. Genera of the phylum Firmicutes are frequently identified as sources of such metabolites, but the biosynthetic potential of its Virgibacillus genus is not known. Here, we used comparative genomic analysis to determine whether Virgibacillus strains isolated from the Red Sea mangrove mud in Rabigh Harbor Lagoon, Saudi Arabia, may be an attractive source of such novel antimicrobial agents.ResultsA comparative genomics analysis based on Virgibacillus dokdonensis Bac330, Virgibacillus sp. Bac332 and Virgibacillus halodenitrificans Bac324 (isolated from the Red Sea) and six other previously reported Virgibacillus strains was performed. Orthology analysis was used to determine the core genomes as well as the accessory genome of the nine Virgibacillus strains. The analysis shows that the Red Sea strain Virgibacillus sp. Bac332 has the highest number of unique genes and genomic islands compared to other genomes included in this study. Focusing on biosynthetic gene clusters, we show how marine isolates, including those from the Red Sea, are more enriched with nonribosomal peptides compared to the other Virgibacillus species. We also found that most nonribosomal peptide synthases identified in the Virgibacillus strains are part of genomic regions that are potentially horizontally transferred.ConclusionsThe Red Sea Virgibacillus strains have a large number of biosynthetic genes in clusters that are not assigned to known products, indicating significant potential for the discovery of novel bioactive compounds. Also, having more modular synthetase units suggests that these strains are good candidates for experimental characterization of previously identified bioactive compounds as well. Future efforts will be directed towards establishing the properties of the potentially novel compounds encoded by the Red Sea specific trans-AT PKS/NRPS cluster and the type III PKS/NRPS cluster.

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Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters.

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Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters.

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