Coherence of <i>Microcystis</i> species revealed through population genomics

Abstract Microcystis is a genus of freshwater cyanobacteria which causes harmful blooms in ecosystems worldwide. Some Microcystis strains produce harmful toxins such as microcystin, impacting drinking water quality. Microcystis colony morphology, rather than genetic similarity, is often used to classify Microcystis into morphospecies. However, colony morphology is a plastic trait which can change depending on environmental and laboratory culture conditions, and is thus an inadequate criterion for species delineation. Furthermore, Microcystis populations are thought to disperse globally and constitute a homogeneous gene pool. However, this assertion is based on relatively incomplete characterization of Microcystis genomic diversity. To better understand these issues, we performed a population genomic analysis of 33 newly sequenced genomes (of which 19 were resequenced to check for mutation in culture) mainly from Canada and Brazil. We identified eight Microcystis clusters of genomic similarity, only four of which correspond to named morphospecies and monophyletic groups. Notably, M. aeruginosa is paraphyletic, distributed across four genomic clusters, suggesting it is not a coherent species. Most monophyletic groups are specific to a unique geographic location, suggesting biogeographic structure over relatively short evolutionary time scales. Higher homologous recombination rates within than between clusters further suggest that monophyletic groups might adhere to a Biological Species-like concept, in which barriers to gene flow maintain species distinctness. However, certain genes – including some involved in microcystin and micropeptin biosynthesis – are recombined between monophyletic groups in the same geographic location, suggesting local adaptation. Together, our results show the importance of using genomic criteria for Microcystis species delimitation and suggest the existence of locally adapted lineages and genes. Importance The genus Microcystis is responsible for harmful and often toxic cyanobacterial blooms across the world, yet it is unclear how and if the genus should be divided into ecologically and genomically distinct species. To resolve the controversy and uncertainty surrounding Microcystis species, we performed a population genomic analysis of Microcystis genome from public databases, along with new isolates from Canada and Brazil. We inferred that significant genetic substructure exists within Microcystis , with several species being maintained by barriers to gene flow. Thus, Microcystis appears to be among a growing number of bacteria that adhere to a Biological Species-like Concept (BSC). Barriers to gene flow are permeable, however, and we find evidence for relatively frequent cross-species horizontal gene transfer (HGT) of genes that may be involved in local adaptation. Distinct clades of Microcystis (putative species) tend to have distinct profiles of toxin biosynthesis genes, and yet toxin genes are also subject to cross-species HGT and local adaptation. Our results thus pave the way for more informed classification, monitoring and understanding of harmful Microcystis blooms.

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