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

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.

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 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 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 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 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.