Quorum sensing signals from epibiont mediate the induction of bioactive peptides in mat-forming cyanobacteria Nostoc

Abstract

The regulation of oligopeptides production is essential in understanding their ecological role in complex microbial communities including harmful cyanobacterial blooms. The role of chemical communication between the cyanobacterium and the microbial community harboured as epibionts within its phycosphere is at an initial stage of research and little is understood about its specificity. Herein, we present insight into the role of a bacterial epibiont in regulating production of cyanobacterial oligopeptides microviridins, well-known elastase inhibitors with presumed anti-grazing effects, in an ecologically important cyanobacterial genus Nostoc. Heterologous expression and identification of specific signal molecules from the epibiont suggest the role of a quorum sensing-based interaction. Further, physiological experiments show an increase in microviridin production without affecting cyanobacterial growth and photosynthetic activity. Simultaneously, oligopeptides presenting a selective inhibition pattern provide support for their specific function in response to the presence of cohabitant epibionts. Thus, the chemical interaction revealed in our study provides an example of an interspecies signalling pathway monitoring the bacterial flora around the cyanobacterial filaments and induction of intrinsic species-specific metabolic responses. IMPORTANCEThe regulation of cyanopeptide production beyond microcystin is essential to understand their ecological role in complex microbial communities, e.g. harmful cyanobacterial blooms. The role of chemical communication between the cyanobacterium and the epibionts within its phycosphere is at an initial stage of research and little is understood about its specificity. The frequency of cyanopeptide occurrence also demonstrates the need to understand the contribution of cyanobacterial peptides to the overall biological impact of cyanopeptides on aquatic organisms and vertebrates including humans. Our results shed light on the epibiont control of cyanopeptide production via quorum sensing mechanisms and we posit that such mechanisms may be widespread in natural cyanobacterial bloom community regulation.