Resource partitioning strategies during toxin production in Microcystis aeruginosa revealed by integrative omics analysis

Abstract

Escalating rates of urbanization and climate change have led to increased occurrence of harmful algal blooms (HABs) in natural waters. HABs caused by Microcystis aeruginosa produce toxic secondary metabolites, such as microcystins (MCs). To understand resource partitioning strategies between cell growth and MC production in response to environmental triggers, we tested the effect of interactions between light and nitrogen on Microcystis aeruginosa PCC 7806. Statistical models revealed that both light and nitrogen affected the transcriptome and metabolome, however, light was the most important of these two factors driving changes at the transcriptome level. On the contrary, effects at metabolome level were less pronounced and were restricted to a few inter-related networks that share rate-limiting substrates and pathway intermediates. Through the integrative systems level approach, we found certain networks belonging to cellular growth, cellular scavenging and secondary metabolites that drive the overall resource partitioning strategy in Microcystis. Additionally, rate limiting metabolites (malonyl-CoA and metabolite couplet SAM; S-adenosyl methionine–SAH; S-S-Adenosyl-L-homocysteine) that occur at the crossroads of the light and nitrogen dependent pathways were identified, thus controlling the metabolic flux and resource allocation in Microcystis cultures. Through these observations, we provide a conceptual model for environmental responses of Microcystis. This model could be validated through controlled feeding experiments and specific genetic mutants to obtain further insights.