Dissolved Organic Matter, Calcium ion and Extracellular Polymeric Substances on Living Associated Bacteria of Microcystis Colony are Crucial for Unicellular Microcystis to Efficiently Form Colonies

Microcystis typically forms colonies under natural conditions, which contributes to occurrence and prevalence of algal blooms. The colonies consist of Microcystis and associated bacteria (AB), embedded in extracellular polymeric substances (EPS). Previous studies indicate that AB can induce Microcystis to form colonies, however the efficiency is generally low and results in a uniform morphotype. In this study, by using filtrated natural water, several AB strains induced unicellular M. aeruginosa to form colonies resembling several Microcystis morphotypes. The mechanisms were investigated with Methylobacterium sp. Z5. Ca2+ was necessary for Z5 to induce Microcystis to form colonies, while dissolved organic matters (DOM) facilitated AB to agglomerate Microcystis to form large colonies. EPS of living Z5, mainly the aromatic protein components, played a key role in colony induction. Z5 initially aggregated Microcystis via the bridging effects of Ca2+ and DOM, followed by the induction of EPS synthesis and secretion in Microcystis. In this process, the colony forming mode shifted from cell adhesion to a combination of cell adhesion and cell division. Intriguingly, Z5 drove the genomic rearrangement of Microcystis by upregulating some transposase genes. This study unveiled a novel mechanism about Microcystis colony formation and identified a new driver of Microcystis genomic evolution. Environmental implication Blooms of cyanobacterium Microcystis are increasing globally, leading to the deterioration of water quality, death of aquatic animals, as well as threats to human health. Microcystis is actually a kind of "hazardous material".Microcystis forms colonies of different sizes and morphologies during blooming. Colonial form endows Microcystis with more resistance to predation and adverse conditions than unicellular Microcystis, which is thought as the prerequisite of Microcystis bloom occurrence and prevalence. This study provides new evidence for understanding the colony forming and morphological shift of Microcystis in natural environment, which will be helpful for developing efficient bloom control strategies.