Spatio-temporal connectivity of a toxic cyanobacterial community and its associated microbiome along a freshwater-marine continuum

• Published in: Harmful algae 2024-04, Vol.134, p.102627, Article 102627
• Main Authors: Reignier, Océane, Bormans, Myriam, Hervé, Fabienne, Robert, Elise, Savar, Véronique, Tanniou, Simon, Amzil, Zouher, Noël, Cyril, Briand, Enora
• Format: Article
• Language: English
• Subjects: Biodiversity and Ecology; Cyanobacteria - genetics; Cyanobacteria - metabolism; Cyanobacteria - physiology; Cyanosphere; Environmental Sciences; France; Fresh Water - microbiology; Harmful Algal Bloom; Microbiota; Microcystins; Microcystins - metabolism; Microcystis - physiology; Microcystis bloom; Osmolytes; Salinity; Seawater - chemistry; Seawater - microbiology
• ISSN: 1568-9883; 1878-1470; 1878-1470
• DOI: 10.1016/j.hal.2024.102627

•M. aeruginosa and M. wesenbergii survived salinities up to 20.•An increase in compatible solutes, particularly trehalose and betaine, occurred along the freshwater-marine continuum.•Salinity played a key role in structuring the heterotrophic bacteria community.•The mucilage-associated microbiome was conserved along the continuum. Due to climate changes and eutrophication, blooms of predominantly toxic freshwater cyanobacteria are intensifying and are likely to colonize estuaries, thus impacting benthic organisms and shellfish farming representing a major ecological, health and economic risk. In the natural environment, Microcystis form large mucilaginous colonies that influence the development of both cyanobacterial and embedded bacterial communities. However, little is known about the fate of natural colonies of Microcystis by salinity increase. In this study, we monitored the fate of a Microcystis dominated bloom and its microbiome along a French freshwater-marine gradient at different phases of a bloom. We demonstrated changes in the cyanobacterial genotypic composition, in the production of specific metabolites (toxins and compatible solutes) and in the heterotrophic bacteria structure in response to the salinity increase. In particular M. aeruginosa and M. wesenbergii survived salinities up to 20. Based on microcystin gene abundance, the cyanobacteria became more toxic during their estuarine transfer but with no selection of specific microcystin variants. An increase in compatible solutes occurred along the continuum with extensive trehalose and betaine accumulations. Salinity structured most the heterotrophic bacteria community, with an increased in the richness and diversity along the continuum. A core microbiome in the mucilage-associated attached fraction was highly abundant suggesting a strong interaction between Microcystis and its microbiome and a likely protecting role of the mucilage against an osmotic shock. These results underline the need to better determine the interactions between the Microcystis colonies and their microbiome as a likely key to their widespread success and adaptation to various environmental conditions.