Authors: Olga M. Pérez-Carrascal, Nicolas Tromas, Yves Terrat, Elisa Moreno, Alessandra Giani, Laisa Corrêa Braga Marques, Nathalie Fortin, B. Jesse Shapiro
Published: 2021-09-27
DOI: 10.1186/s40168-021-01140-8
Source: Full article
AbstractBackgroundCyanobacteria from the genusMicrocystiscan form large mucilaginous colonies with attached heterotrophic bacteria—their microbiome. However, the nature of the relationship betweenMicrocystisand its microbiome remains unclear. Is it a long-term, evolutionarily stable association? Which partners benefit? Here we report the genomic diversity of 109 individualMicrocystiscolonies—including cyanobacteria and associated bacterial genomes—isolatedin situand without culture from Lake Champlain, Canada and Pampulha Reservoir, Brazil.ResultsWe identified 14 distinctMicrocystisgenotypes from Canada, of which only two have been previously reported, and four genotypes specific to Brazil.Microcystisgenetic diversity was much greater between than within colonies, consistent with colony growth by clonal expansion rather than aggregation ofMicrocystiscells. We also identified 72 bacterial species in the microbiome. EachMicrocystisgenotype had a distinct microbiome composition, and more closely related genotypes had more similar microbiomes. This pattern of phylosymbiosis could be explained by co-phylogeny in only two out of the nine most prevalent associated bacterial genera,RoseomonasandRhodobacter. These phylogenetically associated genera could enrich the metabolic repertoire ofMicrocystis,for example by encoding the biosynthesis of complementary carotenoid molecules.In contrast, other colony-associated bacteria showed weaker signals of co-phylogeny, but stronger evidence of horizontal gene transfer withMicrocystis. These observations suggest that acquired genes are more likely to be retained in both partners (Microcystisand members of its microbiome) when they are loosely associated, whereas one gene copy is sufficient when the association is physically tight and evolutionarily long-lasting.ConclusionsWe have introduced a method for culture-free isolation of single colonies from nature followed by metagenomic sequencing, which could be applied to other types of microbes. Together, our results expand the known genetic diversity of bothMicrocystisand its microbiome in natural settings, and support their long-term, specific, and potentially beneficial associations.