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Cited by 222Aquatic Ecosystems and Phytoplankton DynamicsGenomics and Phylogenetic StudiesBacterial Genetics and Biotechnology

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Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium

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Frangeul, Lionel, Quillardet, Philippe, Castets, Anne-Marie, Humbert, Jean-François, Matthijs, Hans CP, Cortez, Diego, Tolonen, Andrew, Zhang, Cheng-Cai, Gribaldo, Simonetta, Kehr, Jan-Christoph, Zilliges, Yvonne, Ziemert, Nadine, Becker, Sven, Talla, Emmanuel, Latifi, Amel, Billault, Alain, Lepelletier, Anthony, Dittmann, Elke, Bouchier, Christiane, Tandeau de Marsac, Nicole·2008·BMC Genomics
DOI 10.1186/1471-2164-9-274PMC PMC2442094
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Abstract

Background: The colonial cyanobacterium Microcystis proliferates in a wide range of freshwater ecosystems and is exposed to changing environmental factors during its life cycle.Microcystis blooms are often toxic, potentially fatal to animals and humans, and may cause environmental problems. There has been little investigation of the genomics of these cyanobacteria. Results: Deciphering the 5,172,804 bp sequence of Microcystis aeruginosa PCC 7806 has revealed the high plasticity of its genome: 11.7% DNA repeats containing more than 1,000 bases, 6.8% putative transposases and 21 putative restriction enzymes. Compared to the genomes of other cyanobacterial lineages, strain PCC 7806 contains a large number of atypical genes that may have been acquired by lateral transfers. Metabolic pathways, such as fermentation and a methionine salvage pathway, have been identified, as have genes for programmed cell death that may be related to the rapid disappearance of Microcystis blooms in nature. Analysis of the PCC 7806 genome also reveals striking novel biosynthetic features that might help to elucidate the ecological impact of secondary metabolites and lead to the discovery of novel metabolites for new biotechnological applications.M. aeruginosa and other large cyanobacterial genomes exhibit a rapid loss of synteny in contrast to other microbial genomes. Conclusion: Microcystis aeruginosa PCC 7806 appears to have adopted an evolutionary strategy relying on unusual genome plasticity to adapt to eutrophic freshwater ecosystems, a property shared by another strain of M. aeruginosa(NIES-843). Comparisons of the genomes of PCC 7806 and other cyanobacterial strains indicate that a similar strategy may have also been used by the marine strain Crocosphaera watsonii WH8501 to adapt to other ecological niches, such as oligotrophic open oceans.

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Figure 1 Phylogenetic maximum likelihood (ML) tree based on the concatenated 23S-16S rDNA sequences of diverse cyanobacterial lineages. The sequences were taken from public databases. Strain identifiers, and the methods used for the phylogenetic analysis, are described in the Methods section. The scale bar represents the average number of nucleotide substitutions per site. Genome sizes in megabases (Mb) are mentioned in parentheses. Trees were constructed using three methods (ML, Neighbor Joining and Maximum Parsimony). ML bootstrap values are indicated only if the bootstrap values obtained with the three methods are > 500 (1000 resamplings).
Figure 1 Phylogenetic maximum likelihood (ML) tree based on the concatenated 23S-16S rDNA sequences of diverse cyanobacterial lineages. The sequences were taken from public databases. Strain identifiers, and the methods used for the phylogenetic analysis, are described in the Methods section. The scale bar represents the average number of nucleotide substitutions per site. Genome sizes in megabases (Mb) are mentioned in parentheses. Trees were constructed using three methods (ML, Neighbor Joining and Maximum Parsimony). ML bootstrap values are indicated only if the bootstrap values obtained with the three methods are > 500 (1000 resamplings).CC BY · PubMed Central
Figure 2 Percentage of DNA repeated sequences in the total genome length. This analysis was performed on complete and in-finishing (*) cyanobacterial genomes. The strain identifiers are listed in the Methods section. Only DNA repeats containing more than 1000 bases, and with an identity threshold >90%, are taken into account.
Figure 2 Percentage of DNA repeated sequences in the total genome length. This analysis was performed on complete and in-finishing (*) cyanobacterial genomes. The strain identifiers are listed in the Methods section. Only DNA repeats containing more than 1000 bases, and with an identity threshold >90%, are taken into account.CC BY · PubMed Central
Figure 3 Comparison of the syntenic scores of cyanobacterial genomes (filled square) and other bacterial genomes (empty diamond) according to the maximum likelihood distances of their 23S-16S sequences calculated by Phyml (see Methods). The pairs of cyanobacterial genomes used in this study are listed in the Methods section.
Figure 3 Comparison of the syntenic scores of cyanobacterial genomes (filled square) and other bacterial genomes (empty diamond) according to the maximum likelihood distances of their 23S-16S sequences calculated by Phyml (see Methods). The pairs of cyanobacterial genomes used in this study are listed in the Methods section.CC BY · PubMed Central
Figure 4 Distribution of the intergenic distances in diverse cyanobacterial genomes. The distances are based on the public syntaxic annotation of each genome. Strain identifiers are listed in the Methods section.
Figure 4 Distribution of the intergenic distances in diverse cyanobacterial genomes. The distances are based on the public syntaxic annotation of each genome. Strain identifiers are listed in the Methods section.CC BY · PubMed Central
Figure 5 Schematic representation of secondary metabolite gene clusters in Mic-PCC7806. (A) Gene clusters encoding non-ribosomal peptide synthetases (NRPS) and polyketide synthases (PKS). The names assigned to individual genes in Mic-PCC7806, or to genes that were characterized in other cyanobacterial strains are indicated above the arrows. Products assigned to the respective pathways are shown on the right. (B) Gene cluster encoding enzymes potentially involved in a patellamide-like pathway. Names of patellamide biosynthesis genes are indicated above the arrows. Gene identifiers in the Mic-PCC7806 genome are indicated below the arrows.
Figure 5 Schematic representation of secondary metabolite gene clusters in Mic-PCC7806. (A) Gene clusters encoding non-ribosomal peptide synthetases (NRPS) and polyketide synthases (PKS). The names assigned to individual genes in Mic-PCC7806, or to genes that were characterized in other cyanobacterial strains are indicated above the arrows. Products assigned to the respective pathways are shown on the right. (B) Gene cluster encoding enzymes potentially involved in a patellamide-like pathway. Names of patellamide biosynthesis genes are indicated above the arrows. Gene identifiers in the Mic-PCC7806 genome are indicated below the arrows.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. Steffensen DA: Economic costs of cyanobacterial blooms. Interagency, International Symposium on Cyanobacterial Harmful Algal Blooms (ISOC-HAB), Advances in Experimental Medicine and Biology. 2008, New York: Springer Verlag, 619: 843-853.

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Metadata

Authors
Frangeul, L., Quillardet, P., Castets, A.-M., Humbert, J.-F., Matthijs, H. C., Cortez, D., Tolonen, A., Zhang, C.-C., Gribaldo, S., Kehr, J.-C., Zilliges, Y., Ziemert, N., Becker, S., Talla, E., Latifi, A., Billault, A., Lepelletier, A., Dittmann, E., Bouchier, C., & Tandeau de Marsac, N.
Affiliations
  • Institut Pasteur (FR)
  • Centre National de la Recherche Scientifique (FR)
  • University of Amsterdam (NL)
  • Humboldt-Universität zu Berlin (DE)
  • Netherlands Institute of Ecology (NL)
  • Genoscope (FR)
ORCID
Venue
BMC Genomics
Publisher
Springer Science and Business Media LLC
Published
2008-06-05
Volume
9
Issue
1
Pages
274-274
ISSN
1471-2164 (ISSN-L)
DOI
10.1186/1471-2164-9-274
PMC
PMC2442094
OpenAlex
W2109250549
Cited by
221
References
81
Citations by year
2026: 6 · 2025: 7 · 2024: 12 · 2023: 10 · 2022: 9 · 2021: 9 · 2020: 7 · 2019: 19 · 2018: 12 · 2017: 9 · 2016: 12 · 2015: 15 · 2014: 20 · 2013: 14 · 2012: 17
FWCI
10.47
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Genomics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UvA-DARE (University of Amsterdam) (publishedVersion, cc-by)
  • KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, cc-by)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
  • Gordon and Betty Moore Foundation
  • Centre National de la Recherche Scientifique
Topics
  • Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
genome plasticity, cyanobacterial genomics, repetitive DNA, transposase, restriction enzymes, horizontal gene transfer, methionine salvage pathway, programmed cell death, cyanobacterial blooms, secondary metabolites, biosynthetic genes
MeSH terms
Animals, DNA, Bacterial, DNA, Ribosomal, Fresh Water, Multigene Family, Humans, Molecular Sequence Data, Phylogeny, Repetitive Sequences, Nucleic Acid, Species Specificity, DNA Restriction-Modification Enzymes, Genome, Bacterial, Ecosystem, Evolution, Molecular, DNA, Intergenic, Microcystis

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