Genome sequences of lower Great Lakes Microcystis sp. reveal strain-specific genes that are present and expressed in western Lake Erie blooms

Abstract

Blooms of the potentially toxic cyanobacterium Microcystis are increasing worldwide. In the Laurentian Great Lakes they pose major socioeconomic, ecological, and human health threats, particularly in western Lake Erie. However, the interpretation of “omics” data is constrained by the highly variable genome of Microcystis and the small number of reference genome sequences from strains isolated from the Great Lakes. To address this, we sequenced two Microcystis isolates from Lake Erie (Microcystis aeruginosa LE3 and M. wesenbergii LE013-01) and one from upstream Lake St. Clair (M. cf aeruginosa LSC13-02), and compared these data to the genomes of seventeen Microcystis spp. from across the globe as well as one metagenome and seven metatranscriptomes from a 2014 Lake Erie Microcystis bloom. For the publically available strains analyzed, the core genome is ~1900 genes, representing ~11% of total genes in the pan-genome and ~45% of each strain’s genome. The flexible genome content was related to Microcystis subclades defined by phylogenetic analysis of both housekeeping genes and total core genes. To our knowledge this is the first evidence that the flexible genome is linked to the core genome of the Microcystis species complex. The majority of strain-specific genes were present and expressed in bloom communities in Lake Erie. Roughly 8% of these genes from the lower Great Lakes are involved in genome plasticity (rapid gain, loss, or rearrangement of genes) and resistance to foreign genetic elements (such as CRISPR-Cas systems). Intriguingly, strain-specific genes from Microcystis cultured from around the world were also present and expressed in the Lake Erie blooms, suggesting that the Microcystis pangenome is truly global. The presence and expression of flexible genes, including strain-specific genes, suggests that strain-level genomic diversity may be important in maintaining Microcystis abundance during bloom events.

Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa

“…Our study broadens understanding of this environmentally important cyanobacterium from genotypes of M. aeruginosa that are adapted to phosphorus-rich environments (Meyer et al, 2017) to genotypes of M. aeruginosa that evidently correspond with survival and colony formation of Microcystis in low-phosphorus environments. Architecture of these genomes is indicative of selective pressure towards more streamlined cellular efficiency.…”

“…Sequenced M. aeruginosa genomes from eutrophic habitats are highly variable, but this variation does not show clear biogeographic patterns (Meyer et al, 2017). In contrast, we previously identified a monophyletic ecotype of M. aeruginosa occurring in oligotrophic inland lakes in Michigan (Berry, White, et al, 2017).…”

“…As a consequence, eutrophic environments have been the focus of genome sequencing effort for M. aeruginosa . Their genomes are noted as having an unusually high percentage of long DNA repeats, insertions, transposable elements and lateral gene transfers (Franguel et al, ; Kaneko et al, ; Meyer et al, ). Sequenced M. aeruginosa genomes from eutrophic habitats are highly variable, but this variation does not show clear biogeographic patterns (Meyer et al, ).…”

“…Their genomes are noted as having an unusually high percentage of long DNA repeats, insertions, transposable elements and lateral gene transfers (Franguel et al, ; Kaneko et al, ; Meyer et al, ). Sequenced M. aeruginosa genomes from eutrophic habitats are highly variable, but this variation does not show clear biogeographic patterns (Meyer et al, ). In contrast, we previously identified a monophyletic ecotype of M. aeruginosa occurring in oligotrophic inland lakes in Michigan (Berry, White, et al, ).…”

“…As a consequence, eutrophic environments have been the focus of genome sequencing effort for M. aeruginosa. Their genomes are noted as having an unusually high percentage of long DNA repeats, insertions, transposable elements and lateral gene transfers (Franguel et al, 2008;Kaneko et al, 2007;Meyer et al, 2017).…”