Quorum sensing regulation in Microcystis aeruginosa: Insights into AHL-mediated physiological processes and MC-LR production

Quorum sensing (QS) is a widespread regulatory mechanism in Gram-negative bacteria, primarily involving the secretion of N-acyl homoserine lactone (AHL) to facilitate population density sensing. However, the existence of QS in blue-green algae, a subset of photoautotrophic Gram-negative bacteria forming high-density communities in water blooms, remains elusive. This study delves into the unexplored realm of QS in Microcystis aeruginosa (M. aeruginosa) by investigating AHL-related regulatory mechanisms and their impact on various physiological processes. Utilizing high-performance liquid chromatography coupled with mass spectrometry (HPLC-MS) and biosensors, a hitherto unknown long-chain AHL exhibiting a mass-to-charge ratio of 318 was identified in sterile M. aeruginosa cultures. Our investigation focused on discerning correlations between AHL activity fluctuations and key parameters such as microcystin (MC-LR) production, algal density, photosynthesis, buoyancy, and aggregation. Furthermore, the AHL extract was introduced during the logarithmic stage of M. aeruginosa cultures to observe the response in physiological processes. The results revealed that AHL, functioning as an autoinducer (AI), positively influenced algal growth and photosynthesis, as evidenced by the upregulated photosynthetic conversion efficiency of PSI and chlorophyll synthesis gene (psbA). AI also played a crucial role in altering surface characteristics through the synthesis of polysaccharides and proteins in EPS, subsequently promoting cell aggregation. Concomitantly, AI upregulated mcyD, enhancing the synthesis of MC-LR. Notably, our investigation pinpointed the initiation of QS in Microcystis at a density of approximately 1.22 × 10^7 cells/mL. This groundbreaking evidence underscores the regulatory role of AI in governing the physiological processes of growth, aggregation, buoyancy, and MC-LR production by activating pertinent gene expressions. This study significantly expands the understanding of QS in AHL, providing crucial insights into the regulatory networks operating in blue-green algae.