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      Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria

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          Abstract

          Background

          Cyanobacteria are an ancient lineage of photosynthetic bacteria from which hundreds of natural products have been described, including many notorious toxins but also potent natural products of interest to the pharmaceutical and biotechnological industries. Many of these compounds are the products of non-ribosomal peptide synthetase (NRPS) or polyketide synthase (PKS) pathways. However, current understanding of the diversification of these pathways is largely based on the chemical structure of the bioactive compounds, while the evolutionary forces driving their remarkable chemical diversity are poorly understood.

          Results

          We carried out a phylum-wide investigation of genetic diversification of the cyanobacterial NRPS and PKS pathways for the production of bioactive compounds. 452 NRPS and PKS gene clusters were identified from 89 cyanobacterial genomes, revealing a clear burst in late-branching lineages. Our genomic analysis further grouped the clusters into 286 highly diversified cluster families (CF) of pathways. Some CFs appeared vertically inherited, while others presented a more complex evolutionary history. Only a few horizontal gene transfers were evidenced amongst strongly conserved CFs in the phylum, while several others have undergone drastic gene shuffling events, which could result in the observed diversification of the pathways.

          Conclusions

          Therefore, in addition to toxin production, several NRPS and PKS gene clusters are devoted to important cellular processes of these bacteria such as nitrogen fixation and iron uptake. The majority of the biosynthetic clusters identified here have unknown end products, highlighting the power of genome mining for the discovery of new natural products.

          Electronic supplementary material

          The online version of this article (doi:10.1186/1471-2164-15-977) contains supplementary material, which is available to authorized users.

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          Most cited references48

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          BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments

          Background The quality of multiple sequence alignments plays an important role in the accuracy of phylogenetic inference. It has been shown that removing ambiguously aligned regions, but also other sources of bias such as highly variable (saturated) characters, can improve the overall performance of many phylogenetic reconstruction methods. A current scientific trend is to build phylogenetic trees from a large number of sequence datasets (semi-)automatically extracted from numerous complete genomes. Because these approaches do not allow a precise manual curation of each dataset, there exists a real need for efficient bioinformatic tools dedicated to this alignment character trimming step. Results Here is presented a new software, named BMGE (Block Mapping and Gathering with Entropy), that is designed to select regions in a multiple sequence alignment that are suited for phylogenetic inference. For each character, BMGE computes a score closely related to an entropy value. Calculation of these entropy-like scores is weighted with BLOSUM or PAM similarity matrices in order to distinguish among biologically expected and unexpected variability for each aligned character. Sets of contiguous characters with a score above a given threshold are considered as not suited for phylogenetic inference and then removed. Simulation analyses show that the character trimming performed by BMGE produces datasets leading to accurate trees, especially with alignments including distantly-related sequences. BMGE also implements trimming and recoding methods aimed at minimizing phylogeny reconstruction artefacts due to compositional heterogeneity. Conclusions BMGE is able to perform biologically relevant trimming on a multiple alignment of DNA, codon or amino acid sequences. Java source code and executable are freely available at ftp://ftp.pasteur.fr/pub/GenSoft/projects/BMGE/.
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            Mass spectral molecular networking of living microbial colonies.

            Integrating the governing chemistry with the genomics and phenotypes of microbial colonies has been a "holy grail" in microbiology. This work describes a highly sensitive, broadly applicable, and cost-effective approach that allows metabolic profiling of live microbial colonies directly from a Petri dish without any sample preparation. Nanospray desorption electrospray ionization mass spectrometry (MS), combined with alignment of MS data and molecular networking, enabled monitoring of metabolite production from live microbial colonies from diverse bacterial genera, including Bacillus subtilis, Streptomyces coelicolor, Mycobacterium smegmatis, and Pseudomonas aeruginosa. This work demonstrates that, by using these tools to visualize small molecular changes within bacterial interactions, insights can be gained into bacterial developmental processes as a result of the improved organization of MS/MS data. To validate this experimental platform, metabolic profiling was performed on Pseudomonas sp. SH-C52, which protects sugar beet plants from infections by specific soil-borne fungi [R. Mendes et al. (2011) Science 332:1097-1100]. The antifungal effect of strain SH-C52 was attributed to thanamycin, a predicted lipopeptide encoded by a nonribosomal peptide synthetase gene cluster. Our technology, in combination with our recently developed peptidogenomics strategy, enabled the detection and partial characterization of thanamycin and showed that it is a monochlorinated lipopeptide that belongs to the syringomycin family of antifungal agents. In conclusion, the platform presented here provides a significant advancement in our ability to understand the spatiotemporal dynamics of metabolite production in live microbial colonies and communities.
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              Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing.

              The cyanobacterial phylum encompasses oxygenic photosynthetic prokaryotes of a great breadth of morphologies and ecologies; they play key roles in global carbon and nitrogen cycles. The chloroplasts of all photosynthetic eukaryotes can trace their ancestry to cyanobacteria. Cyanobacteria also attract considerable interest as platforms for "green" biotechnology and biofuels. To explore the molecular basis of their different phenotypes and biochemical capabilities, we sequenced the genomes of 54 phylogenetically and phenotypically diverse cyanobacterial strains. Comparison of cyanobacterial genomes reveals the molecular basis for many aspects of cyanobacterial ecophysiological diversity, as well as the convergence of complex morphologies without the acquisition of novel proteins. This phylum-wide study highlights the benefits of diversity-driven genome sequencing, identifying more than 21,000 cyanobacterial proteins with no detectable similarity to known proteins, and foregrounds the diversity of light-harvesting proteins and gene clusters for secondary metabolite biosynthesis. Additionally, our results provide insight into the distribution of genes of cyanobacterial origin in eukaryotic nuclear genomes. Moreover, this study doubles both the amount and the phylogenetic diversity of cyanobacterial genome sequence data. Given the exponentially growing number of sequenced genomes, this diversity-driven study demonstrates the perspective gained by comparing disparate yet related genomes in a phylum-wide context and the insights that are gained from it.
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                Author and article information

                Contributors
                acalteau@genoscope.cns.fr
                david.fewer@helsinki.fi
                latifi@ifr88.cnrs-mrs.fr
                therese.coursin@pasteur.fr
                thierry.laurent@pasteur.fr
                jouni.jokela@helsinki.fi
                ckerfeld@lbl.gov
                kaarina.sivonen@helsinki.fi
                jpiel@ethz.ch
                mgugger@pasteur.fr
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                18 November 2014
                18 November 2014
                2014
                : 15
                : 1
                : 977
                Affiliations
                [ ]Commissariat à l’Energie Atomique et aux Energies Alternatives (CEA), Genoscope & CNRS, UMR 8030, Laboratoire d’Analyse Bioinformatique en Génomique et Métabolisme, Evry, France
                [ ]Department of Food and Environmental Sciences, University of Helsinki, Helsinki, Finland
                [ ]Centre National de la Recherche Scientifique (CNRS), Aix-Marseille University, Marseille, France
                [ ]Institut Pasteur, Collection des Cyanobactéries, Paris, France
                [ ]Department of Plant and Microbial Biology, University of California, Berkeley, CA USA
                [ ]DOE Plant Research Center, Michigan State University, Michigan, MI USA
                [ ]Institute of Microbiology, Eidgenoessiche Technische Hochschule (ETH), Zurich, Switzerland
                Article
                6690
                10.1186/1471-2164-15-977
                4247773
                25404466
                5e205648-8980-4589-8e01-c98a97e3fb06
                © Calteau et al.; licensee BioMed Central Ltd. 2014

                This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 25 July 2014
                : 30 October 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                cyanobacteria,secondary metabolite,nrps,pks,diversity,evolution
                Genetics
                cyanobacteria, secondary metabolite, nrps, pks, diversity, evolution

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