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

Abstract

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 devotedmore » 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.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [2];  [5];  [2];  [6];  [4]
+ Show Author Affiliations
  1. Lab. d'Analyse Bioinformatique en Genomique et Metabolisme, Evry (France)
  2. Univ. of Helsinki, Helsinki (Finland)
  3. Aix-Marseille Univ., Marseille (France)
  4. Institut Pasteur, Paris (France)
  5. Univ. of California, Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States)
  6. Eidgenoessiche Technische Hochschule (ETH), Zurich (Switzerland)
Publication Date:
Research Org.:
University of California, Berkeley, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1221960
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cyanobacteria; secondary metabolite; NRPS; PKS; diversity; evolution

Citation Formats

Calteau, Alexandra, Fewer, David P., Latifi, Amel, Coursin, Thérèse, Laurent, Thierry, Jokela, Jouni, Kerfeld, Cheryl A., Sivonen, Kaarina, Piel, Jörn, and Gugger, Muriel. Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria. United States: N. p., 2014. Web. doi:10.1186/1471-2164-15-977.
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Calteau, Alexandra, Fewer, David P., Latifi, Amel, Coursin, Thérèse, Laurent, Thierry, Jokela, Jouni, Kerfeld, Cheryl A., Sivonen, Kaarina, Piel, Jörn, & Gugger, Muriel. Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria. United States. https://doi.org/10.1186/1471-2164-15-977
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Calteau, Alexandra, Fewer, David P., Latifi, Amel, Coursin, Thérèse, Laurent, Thierry, Jokela, Jouni, Kerfeld, Cheryl A., Sivonen, Kaarina, Piel, Jörn, and Gugger, Muriel. Tue . "Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria". United States. https://doi.org/10.1186/1471-2164-15-977. https://www.osti.gov/servlets/purl/1221960.
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@article{osti_1221960,
title = {Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria},
author = {Calteau, Alexandra and Fewer, David P. and Latifi, Amel and Coursin, Thérèse and Laurent, Thierry and Jokela, Jouni and Kerfeld, Cheryl A. and Sivonen, Kaarina and Piel, Jörn and Gugger, Muriel},
abstractNote = {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.},
doi = {10.1186/1471-2164-15-977},
journal = {BMC Genomics},
number = 1,
volume = 15,
place = {United States},
year = {Tue Nov 18 00:00:00 EST 2014},
month = {Tue Nov 18 00:00:00 EST 2014}
}
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Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations
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Mass spectral molecular networking of living microbial colonies
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Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing
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Metagenomic natural product discovery in lichen provides evidence for a family of biosynthetic pathways in diverse symbioses
journal, July 2013

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  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 33
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Diversity and evolution of secondary metabolism in the marine actinomycete genus Salinispora
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MAFFT version 5: improvement in accuracy of multiple sequence alignment
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NRPSpredictor2—a web server for predicting NRPS adenylation domain specificity
journal, May 2011

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antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences
journal, June 2011

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MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data
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New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
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Microcystin Production in the Tripartite Cyanolichen Peltigera leucophlebia
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Unravelling the genomic mosaic of a ubiquitous genus of marine cyanobacteria
journal, January 2008

  • Dufresne, Alexis; Ostrowski, Martin; Scanlan, David J.
  • Genome Biology, Vol. 9, Issue 5
  • DOI: 10.1186/gb-2008-9-5-r90

Natural Biocombinatorics in the Polyketide Synthase Genes of the Actinobacterium Streptomyces avermitilis
journal, January 2006

Origin of Saxitoxin Biosynthetic Genes in Cyanobacteria
journal, June 2009

Widespread Occurrence of Secondary Lipid Biosynthesis Potential in Microbial Lineages
journal, May 2011

A Tribute to Disorder in the Genome of the Bloom-Forming Freshwater Cyanobacterium Microcystis aeruginosa
journal, August 2013

Anachelin, the Siderophore of the Cyanobacterium Anabaena cylindrica CCAP 1403/2A
journal, October 2000

  • Beiderbeck, Hans; Taraz, Kambiz; Budzikiewicz, Herbert
  • Zeitschrift für Naturforschung C, Vol. 55, Issue 9-10
  • DOI: 10.1515/znc-2000-9-1002

MS/MS networking guided analysis of molecule and gene cluster families
text, January 2013

  • M., Gutierrez,; S., Moore, B.; C., Dorrestein, P.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/bd99-qk88

Marine Sponges: Potential Sources of New Antimicrobial Drugs
journal, January 2009

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    Works referencing / citing this record:

    Genome mining for natural product biosynthetic gene clusters in the Subsection V cyanobacteria
    journal, September 2015

    Distribution of Hydrogenases in Cyanobacteria: A Phylum-Wide Genomic Survey
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    Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria
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    Geosmin attracts Aedes aegypti mosquitoes to oviposition sites
    posted_content, January 2019

    • Melo, Nadia; Wolff, Gabriella H.; Costa-da-Silva, Andre Luis
    • bioRxiv
    • DOI: 10.1101/598698

    Cyanobacterial Siderophores—Physiology, Structure, Biosynthesis, and Applications
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    • Årstøl, Erland; Hohmann-Marriott, Martin F.
    • Marine Drugs, Vol. 17, Issue 5
    • DOI: 10.3390/md17050281

    Discovery Strategies of Bioactive Compounds Synthesized by Nonribosomal Peptide Synthetases and Type-I Polyketide Synthases Derived from Marine Microbiomes
    journal, April 2016

    • Amoutzias, Grigoris; Chaliotis, Anargyros; Mossialos, Dimitris
    • Marine Drugs, Vol. 14, Issue 4
    • DOI: 10.3390/md14040080

    Trichophycin A, a Cytotoxic Linear Polyketide Isolated from a Trichodesmium thiebautii Bloom
    journal, January 2017

    • Bertin, Matthew; Wahome, Paul; Zimba, Paul
    • Marine Drugs, Vol. 15, Issue 1
    • DOI: 10.3390/md15010010

    Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
    journal, August 2015

    • Schirrmeister, Bettina E.; Gugger, Muriel; Donoghue, Philip C.
    • Palaeontology, Vol. 58, Issue 5
    • DOI: 10.1111/pala.12193

    Impacts of microbial assemblage and environmental conditions on the distribution of anatoxin-a producing cyanobacteria within a river network
    journal, February 2019

    • Bouma-Gregson, Keith; Olm, Matthew R.; Probst, Alexander J.
    • The ISME Journal, Vol. 13, Issue 6
    • DOI: 10.1038/s41396-019-0374-3

    A Novel Cyanobacterium Synechococcus elongatus PCC 11802 has Distinct Genomic and Metabolomic Characteristics Compared to its Neighbor PCC 11801
    journal, January 2020

    Evolution of Anabaenopeptin Peptide Structural Variability in the Cyanobacterium Planktothrix
    journal, February 2017

    • Entfellner, Elisabeth; Frei, Mark; Christiansen, Guntram
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.00219

    Interpreting Microbial Biosynthesis in the Genomic Age: Biological and Practical Considerations
    journal, June 2017

    • Miller, Ian; Chevrette, Marc; Kwan, Jason
    • Marine Drugs, Vol. 15, Issue 6
    • DOI: 10.3390/md15060165

    Gifted microbes for genome mining and natural product discovery
    journal, August 2016

    Comparative Genomics of Cyanobacterial Symbionts Reveals Distinct, Specialized Metabolism in Tropical Dysideidae Sponges
    journal, May 2019

    • Schorn, Michelle A.; Jordan, Peter A.; Podell, Sheila
    • mBio, Vol. 10, Issue 3
    • DOI: 10.1128/mbio.00821-19

    Heterologous expression and biochemical characterisation of cyanotoxin biosynthesis pathways
    journal, January 2019

    • Cullen, Alescia; Pearson, Leanne A.; Mazmouz, Rabia
    • Natural Product Reports, Vol. 36, Issue 8
    • DOI: 10.1039/c8np00063h

    Insights into the Cyanobacterial Deg/HtrA Proteases
    journal, May 2016

    Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
    journal, June 2015

    • Schirrmeister, Bettina E.; Gugger, Muriel; Donoghue, Philip C. J.
    • Palaeontology, Vol. 58, Issue 5
    • DOI: 10.1111/pala.12178

    High-Density Cultivation of Terrestrial Nostoc Strains Leads to Reprogramming of Secondary Metabolome
    journal, September 2017

    • Guljamow, Arthur; Kreische, Marco; Ishida, Keishi
    • Applied and Environmental Microbiology, Vol. 83, Issue 23
    • DOI: 10.1128/aem.01510-17

    A novel salt-tolerant genotype illuminates the sucrose gene evolution in freshwater bloom-forming cyanobacterium Microcystis aeruginosa
    journal, August 2019

    • Tanabe, Yuuhiko; Yamaguchi, Haruyo; Sano, Tomoharu
    • FEMS Microbiology Letters, Vol. 366, Issue 15
    • DOI: 10.1093/femsle/fnz190

    Phylum-wide analysis of genes/proteins related to the last steps of assembly and export of extracellular polymeric substances (EPS) in cyanobacteria
    journal, October 2015

    • Pereira, Sara B.; Mota, Rita; Vieira, Cristina P.
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep14835

    Bioprospecting Sponge-Associated Marine Cyanobacteria to Produce Bioactive Compounds
    journal, January 2020

    • Konstantinou, Despoina; Mavrogonatou, Eleni; Zervou, Sevasti-Kiriaki
    • Toxins, Vol. 12, Issue 2
    • DOI: 10.3390/toxins12020073

    Physiological and Evolutionary Implications of Tetrameric Photosystem I in Cyanobacteria
    posted_content, February 2019

    • Li, Meng; Calteau, Alexandra; Semchonok, Dmitry A.
    • Nature Plants
    • DOI: 10.1101/544353

    Retrospective analysis of natural products provides insights for future discovery trends
    journal, May 2017

    • Pye, Cameron R.; Bertin, Matthew J.; Lokey, R. Scott
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 22
    • DOI: 10.1073/pnas.1614680114

    Structural and functional analysis of the finished genome of the recently isolated toxic Anabaena sp. WA102
    journal, June 2016

    Modules of co-occurrence in the cyanobacterial pan-genome reveal functional associations between groups of ortholog genes
    journal, March 2018

    The influence of sigma factors and ribosomal recognition elements on heterologous expression of cyanobacterial gene clusters in Escherichia coli
    journal, June 2018

    • Wells, Kaitlyn N.; Videau, Patrick; Nelson, Dylan
    • FEMS Microbiology Letters, Vol. 365, Issue 15
    • DOI: 10.1093/femsle/fny164

    Comparative genomics uncovers the prolific and distinctive metabolic potential of the cyanobacterial genus Moorea
    journal, March 2017

    • Leao, Tiago; Castelão, Guilherme; Korobeynikov, Anton
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
    • DOI: 10.1073/pnas.1618556114

    Cyanobacterial diversity held in microbial biological resource centers as a biotechnological asset: the case study of the newly established LEGE culture collection
    journal, January 2018

    • Ramos, Vitor; Morais, João; Castelo-Branco, Raquel
    • Journal of Applied Phycology, Vol. 30, Issue 3
    • DOI: 10.1007/s10811-017-1369-y

    Data from: Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria
    dataset, January 2015

    Data from: Phylum-wide comparative genomics unravel the diversity of secondary metabolism in Cyanobacteria
    dataset, January 2015

    Cyanobacterial diversity held in microbial biological resource centers as a biotechnological asset: the case study of the newly established LEGE culture collection
    journal, January 2018

    • Ramos, Vitor; Morais, João; Castelo-Branco, Raquel
    • Journal of Applied Phycology, Vol. 30, Issue 3
    • DOI: 10.1007/s10811-017-1369-y

    Geosmin Attracts Aedes aegypti Mosquitoes to Oviposition Sites
    journal, January 2020

    • Melo, Nadia; Wolff, Gabriella H.; Costa-da-Silva, Andre Luis
    • Current Biology, Vol. 30, Issue 1
    • DOI: 10.1016/j.cub.2019.11.002

    A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle
    journal, June 2018

    A Novel Cyanobacterium Synechococcus elongatus PCC 11802 has Distinct Genomic and Metabolomic Characteristics Compared to its Neighbor PCC 11801
    journal, January 2020

    Phylum-wide analysis of genes/proteins related to the last steps of assembly and export of extracellular polymeric substances (EPS) in cyanobacteria
    journal, October 2015

    • Pereira, Sara B.; Mota, Rita; Vieira, Cristina P.
    • Scientific Reports, Vol. 5, Issue 1
    • DOI: 10.1038/srep14835

    Genome mining unveils widespread natural product biosynthetic capacity in human oral microbe Streptococcus mutans
    journal, November 2016

    • Liu, Liwei; Hao, Tingting; Xie, Zhoujie
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep37479

    A Machine Learning Method for Detecting Autocorrelation of Evolutionary Rates in Large Phylogenies
    journal, January 2019

    • Tao, Qiqing; Tamura, Koichiro; U. Battistuzzi, Fabia
    • Molecular Biology and Evolution, Vol. 36, Issue 4
    • DOI: 10.1093/molbev/msz014

    Modules of co-occurrence in the cyanobacterial pan-genome
    posted_content, May 2017

    • Beck, Christian; Knoop, Henning; Steuer, Ralf
    • bioRxiv
    • DOI: 10.1101/137398

    Recovering genomic clusters of secondary metabolites from lakes: a Metagenomics 2.0 approach
    posted_content, August 2017

    • Cuadrat, Rafael R. C.; Ionescu, Danny; Davila, Alberto M. R.
    • bioRxiv
    • DOI: 10.1101/183061

    A new method for detecting autocorrelation of evolutionary rates in large phylogenies
    journal, October 2018

    • Tao, Qiqing; Tamura, Koichiro; Battistuzzi, FAbia
    • Molecular Biology and Evolution
    • DOI: 10.1101/346635

    Physiological and Evolutionary Implications of Tetrameric Photosystem I in Cyanobacteria
    posted_content, February 2019

    • Li, Meng; Calteau, Alexandra; Semchonok, Dmitry A.
    • Nature Plants
    • DOI: 10.1101/544353

    Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
    journal, August 2015

    • Schirrmeister, Bettina E.; Gugger, Muriel; Donoghue, Philip C.
    • Palaeontology, Vol. 58, Issue 5
    • DOI: 10.1111/pala.12193

    Genome mining for natural product biosynthetic gene clusters in the Subsection V cyanobacteria
    journal, September 2015

    Structural and functional analysis of the finished genome of the recently isolated toxic Anabaena sp. WA102
    journal, June 2016

    Modules of co-occurrence in the cyanobacterial pan-genome reveal functional associations between groups of ortholog genes
    journal, March 2018

    The most important marine bacterial toxins; a review
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    Cyanobacterial Toxins of the Laurentian Great Lakes, their Toxicological Effects, and Numerical Limits in Drinking Water
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    Beyond Microcystins: Cyanobacterial Extracts Induce Cytoskeletal Alterations in Rice Root Cells
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    Recovering genomics clusters of secondary metabolites from lakes using genome-resolved metagenomics
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    Distribution of Hydrogenases in Cyanobacteria: A Phylum-Wide Genomic Survey
    journal, December 2016

    Evolution of Anabaenopeptin Peptide Structural Variability in the Cyanobacterium Planktothrix
    journal, February 2017

    • Entfellner, Elisabeth; Frei, Mark; Christiansen, Guntram
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.00219

    A Metagenomic Approach to Cyanobacterial Genomics
    journal, May 2017

    • Alvarenga, Danillo O.; Fiore, Marli F.; Varani, Alessandro M.
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.00809

    Genomic and Genotypic Characterization of Cylindrospermopsis raciborskii: Toward an Intraspecific Phylogenetic Evaluation by Comparative Genomics
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    • Abreu, Vinicius A. C.; Popin, Rafael V.; Alvarenga, Danillo O.
    • Frontiers in Microbiology, Vol. 9
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    Comparative Genomics Discloses the Uniqueness and the Biosynthetic Potential of the Marine Cyanobacterium Hyella patelloides
    journal, July 2020

    Tiny Microbes with a Big Impact: The Role of Cyanobacteria and Their Metabolites in Shaping Our Future
    journal, May 2016

    • Mazard, Sophie; Penesyan, Anahit; Ostrowski, Martin
    • Marine Drugs, Vol. 14, Issue 5
    • DOI: 10.3390/md14050097

    Trichophycin A, a Cytotoxic Linear Polyketide Isolated from a Trichodesmium thiebautii Bloom
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    • Bertin, Matthew; Wahome, Paul; Zimba, Paul
    • Marine Drugs, Vol. 15, Issue 1
    • DOI: 10.3390/md15010010

    Interpreting Microbial Biosynthesis in the Genomic Age: Biological and Practical Considerations
    journal, June 2017

    • Miller, Ian; Chevrette, Marc; Kwan, Jason
    • Marine Drugs, Vol. 15, Issue 6
    • DOI: 10.3390/md15060165

    Cyanobacterial Siderophores—Physiology, Structure, Biosynthesis, and Applications
    journal, May 2019

    • Årstøl, Erland; Hohmann-Marriott, Martin F.
    • Marine Drugs, Vol. 17, Issue 5
    • DOI: 10.3390/md17050281

    Bioprospecting Sponge-Associated Marine Cyanobacteria to Produce Bioactive Compounds
    journal, January 2020

    • Konstantinou, Despoina; Mavrogonatou, Eleni; Zervou, Sevasti-Kiriaki
    • Toxins, Vol. 12, Issue 2
    • DOI: 10.3390/toxins12020073
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