Microdiversity drives resilience and niche partitioning in the bloom forming cyanobacteria Limnospira platensis

Abstract

The intraspecific evolutionary mechanisms of adaptation in blooming cyanobacteria, particularly those occurring on small spatial and temporal scales, remain poorly understood. Here, we used the unique properties of Lake Dziani Dzaha, which hosts a persistent population of Limnospira platensis inhabiting distinct macro-habitats, to explore the spatial and temporal dynamics of microevolution. The Lake Dziani Dzaha (Mayotte), very stable at least since 2010, has experienced a seismo-volcanic crisis from May 2018 to November 2019, characterized by CO2 outgassing that led to the mixing of the initially seasonally stratified water column, as well as changes in numerous physicochemical parameters. Phylogenomic analysis of 108 strains isolated during sampling campaigns in 2010, 2014, 2022, and 2024 revealed a population that remained highly phylogenetically cohesive over time. In 2022, genomic expansion was observed, characterized by an increase in genome size due to the proliferation of insertion sequences and a subsequent loss of adaptive genes. By 2024, a rapid recovery of the 2010-2014 genetic content took place through multiple independent events of horizontal gene transfer. At the spatial scale, although no significant differences in gene content were detected, distinct subpopulations were identified based on allele frequencies. Some alleles were specifically fixed and subject to different selection pressures among the subpopulations, suggesting the existence of distinct ecotypes. Overall, this study highlights the role of microdiversity in rapid resilience of blooming cyanobacteria populations within dynamic environments and in their adaptation through niche partitioning.