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

Calteau, Alexandra; Fewer, David P.; Latifi, Amel; Coursin, Thérèse; Laurent, Thierry; Jokela, Jouni; Kerfeld, Cheryl A.; Sivonen, Kaarina; Piel, Jörn; Gugger, Muriel

doi:10.1186/1471-2164-15-977

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

Journal Article · Tue Nov 18 00:00:00 EST 2014 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-15-977· OSTI ID:1221960

Calteau, Alexandra ^[1]; Fewer, David P. ^[2]; Latifi, Amel ^[3]; Coursin, Thérèse ^[4]; Laurent, Thierry ^[4]; Jokela, Jouni ^[2]; Kerfeld, Cheryl A. ^[5]; Sivonen, Kaarina ^[2]; Piel, Jörn ^[6]; Gugger, Muriel ^[4]

Lab. d'Analyse Bioinformatique en Genomique et Metabolisme, Evry (France)
Univ. of Helsinki, Helsinki (Finland)
Aix-Marseille Univ., Marseille (France)
Institut Pasteur, Paris (France)
Univ. of California, Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States)
Eidgenoessiche Technische Hochschule (ETH), Zurich (Switzerland)

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. 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. 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.

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Research Organization:: University of California, Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1221960

Journal Information:: BMC Genomics, Vol. 15, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 111 works

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The influence of sigma factors and ribosomal recognition elements on heterologous expression of cyanobacterial gene clusters in Escherichia coli Wells, Kaitlyn N.; Videau, Patrick; Nelson, Dylan FEMS Microbiology Letters, Vol. 365, Issue 15 https://doi.org/10.1093/femsle/fny164	journal	June 2018
Comparative genomics uncovers the prolific and distinctive metabolic potential of the cyanobacterial genus Moorea Leao, Tiago; Castelão, Guilherme; Korobeynikov, Anton Proceedings of the National Academy of Sciences, Vol. 114, Issue 12 https://doi.org/10.1073/pnas.1618556114	journal	March 2017
Cyanobacterial diversity held in microbial biological resource centers as a biotechnological asset: the case study of the newly established LEGE culture collection Ramos, Vitor; Morais, João; Castelo-Branco, Raquel Journal of Applied Phycology, Vol. 30, Issue 3 https://doi.org/10.1007/s10811-017-1369-y	journal	January 2018
Data from: Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria Calteau, Alexandra; Fewer, David P.; Latifi, Amel Dryad https://doi.org/10.5061/dryad.p680f	dataset	January 2015
Geosmin Attracts Aedes aegypti Mosquitoes to Oviposition Sites Melo, Nadia; Wolff, Gabriella H.; Costa-da-Silva, Andre Luis Current Biology, Vol. 30, Issue 1 https://doi.org/10.1016/j.cub.2019.11.002	journal	January 2020
A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle Partensky, Frédéric; Six, Christophe; Ratin, Morgane Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-27542-7	journal	June 2018
Genome Features and Biochemical Characteristics of a Robust, Fast Growing and Naturally Transformable Cyanobacterium Synechococcus elongatus PCC 11801 Isolated from India Jaiswal, Damini; Sengupta, Annesha; Sohoni, Sujata Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34872-z	journal	November 2018
Genome mining unveils widespread natural product biosynthetic capacity in human oral microbe Streptococcus mutans Liu, Liwei; Hao, Tingting; Xie, Zhoujie Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep37479	journal	November 2016
A Machine Learning Method for Detecting Autocorrelation of Evolutionary Rates in Large Phylogenies Tao, Qiqing; Tamura, Koichiro; U. Battistuzzi, Fabia Molecular Biology and Evolution, Vol. 36, Issue 4 https://doi.org/10.1093/molbev/msz014	journal	January 2019
Modules of co-occurrence in the cyanobacterial pan-genome Beck, Christian; Knoop, Henning; Steuer, Ralf bioRxiv https://doi.org/10.1101/137398	posted_content	May 2017
Recovering genomic clusters of secondary metabolites from lakes: a Metagenomics 2.0 approach Cuadrat, Rafael R. C.; Ionescu, Danny; Davila, Alberto M. R. bioRxiv https://doi.org/10.1101/183061	posted_content	August 2017
A new method for detecting autocorrelation of evolutionary rates in large phylogenies Tao, Qiqing; Tamura, Koichiro; Battistuzzi, FAbia Molecular Biology and Evolution https://doi.org/10.1101/346635	journal	October 2018
The most important marine bacterial toxins; a review Najafi, Akram; Nabipour, Iraj Iranian South Medical Journal, Vol. 19, Issue 3 https://doi.org/10.18869/acadpub.ismj.19.3.482	journal	July 2016
Cyanobacterial Toxins of the Laurentian Great Lakes, their Toxicological Effects, and Numerical Limits in Drinking Water Miller, Todd R.; Beversdorf, Lucas J.; Weirich, Chelsea A. Preprints.org https://doi.org/10.20944/preprints201703.0148.v1	journal	March 2017
Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells Pappas, Dimitris; Panou, Manthos; Adamakis, Ioannis-Dimosthenis S. Preprints.org https://doi.org/10.20944/preprints202011.0659.v1	journal	November 2020
Recovering genomics clusters of secondary metabolites from lakes using genome-resolved metagenomics Cuadrat, Rafael R. C.; Ionescu, Danny; Dávila, Alberto M. R. Universität Potsdam https://doi.org/10.25932/publishup-44565	text	January 2020
A Metagenomic Approach to Cyanobacterial Genomics Alvarenga, Danillo O.; Fiore, Marli F.; Varani, Alessandro M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00809	journal	May 2017
Genomic and Genotypic Characterization of Cylindrospermopsis raciborskii: Toward an Intraspecific Phylogenetic Evaluation by Comparative Genomics Abreu, Vinicius A. C.; Popin, Rafael V.; Alvarenga, Danillo O. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00306	journal	February 2018
Comparative Genomics Discloses the Uniqueness and the Biosynthetic Potential of the Marine Cyanobacterium Hyella patelloides Brito, Ângela; Vieira, Jorge; Vieira, Cristina P. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01527	journal	July 2020
Tiny Microbes with a Big Impact: The Role of Cyanobacteria and Their Metabolites in Shaping Our Future Mazard, Sophie; Penesyan, Anahit; Ostrowski, Martin Marine Drugs, Vol. 14, Issue 5 https://doi.org/10.3390/md14050097	journal	May 2016

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

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