Microcystin-Driven Control of the Carbon-Concentrating Mechanism Shapes CO2 Fixation Dynamics in Microcystis aeruginosa PCC 7806

Abstract

Bloom-forming cyanobacteria thrive in highly dynamic light environments, yet the mechanisms enabling rapid acclimation to fluctuating irradiance remain poorly understood. Here, we compared light acclimation in the bloom-forming cyanobacterium Microcystis aeruginosa PCC 7806 and the non-bloom-forming model cyanobacterium Synechocystis sp. PCC 6803 and investigated the role of the cyanobacterial toxin microcystin (MC) and its in vivo binding partner RubisCO in this process. Whereas Synechocystis grew faster under sustained high light, Microcystis performed better under low light and responded to transient high-light exposure with a remarkably rapid increase in photosynthetic activity and glycogen accumulation. These responses were markedly attenuated in an MC-deficient mutant. Although RubisCO from Microcystis exhibited pronounced light-dependent changes in activity, MC had only minor effects on RubisCO catalysis, arguing against a direct role in regulating enzyme function. Instead, extracellular MC elicited a transient transcriptional program characterized by induction of inorganic carbon acquisition systems, including the high-affinity bicarbonate transporter BCT1, consistent with activation of the carbon-concentrating mechanism (CCM) and enhanced carbon fixation in vivo. MC further stimulated the expression of photosynthesis-related genes, and altered carboxysome organization, and promoted extracarboxysomal localization of RubisCO. Together, our findings identify MC as a light-responsive signaling molecule that coordinates CCM activity, carbon acquisition, and photosynthetic acclimation, thereby enhancing adaptation of Microcystis to fluctuating irradiance and potentially contributing to its ecological success in cyanobacterial blooms.