Thermal boundaries and underlying systems biology mechanisms in two waterbloom cyanobacteria

Abstract

Climate change and recent heatwaves have elevated temperature to the level of nutrients in driving CHABs. In this new dimension of CHABs ecology, it is important to understand the thermal boundaries of each blooming species. One well-known example is the temporal and thermal partitioning between filamentous, nitrogen-fixing taxa such as Dolichospermum spp. and Pseudanabaena spp., which dominate in spring, and colonial/coccoid Microcystis aeruginosa, which predominates in summer and autumn. Here we show that Dolichospermum sp. and M. aeruginosa display converse temperature-growth relations, Dolichospermum sp. grows better at low temperatures (13-15{degrees}C) and M. aeruginosa grows better at high temperatures (29-31{degrees}C), with similar growth rates between 18 and 25{degrees}C. This thermal separation is sustained by systems-level changes, in terms of the macromolecule contents--proteins, ATP, carbohydrates, and lipids--and transcriptome and metabolic fluxes to critical unsaturated fatty acids, which were experimentally verified by supplementing these FAs. The gene regulatory and systems biology mechanisms are explored. Through homologous and evolutionary analyses, a conserved Hik34-Rre1-RpoD cascade underlying differential temperature-responsive gene regulation. Enzyme-constrained metabolic models reproduced genus-specific lipid shifts and uncovered contrasting flux reorganizations under thermal stress. Together, these results establish the metabolic and regulatory foundations that shape the distinct thermal niches of bloom-forming cyanobacteria, providing mechanistic insight into how climate warming may restructure their seasonal dominance.