Interspecific Interactions Drive Nonribosomal Peptide Production in Nodularia spumigena

Nodularia spumigena is a bloom-forming cyanobacterium that produces several classes of nonribosomal peptides (NRPs) that are biologically active; however, the ecological roles of specific NRPs remain largely unknown. Here, we explored the involvement of NRPs produced by N. spumigena in interspecific interactions by coculturing the cyanobacterium and its algal competitors, the diatom Phaeodactylum tricornutum and the cryptomonad Rhodomonas salina, and measuring NRP levels and growth responses in all three species. Contrary to the expected growth suppression in the algae, it was N. spumigena that was adversely affected by the diatom, while the cryptomonad had no effect. Reciprocal effects of N. spumigena on the algae were manifested as the prolonged lag phase in R. salina and growth stimulation in P. tricornutum; however, these responses were largely attributed to elevated pH and not to specific NRPs. Nevertheless, the NRP levels in the cocultures were significantly higher than in the monocultures, with an up to 5-fold upregulation of cell-bound nodularins and exudation of nodularin and anabaenopeptin. Thus, chemically mediated interspecific interactions can promote NRP production and release by cyanobacteria, resulting in increased input of these compounds into the water. IMPORTANCE NRPs were involved in growth responses of both cyanobacteria and algae; however, the primary driver of the growth trajectories was high pH induced by N. spumigena. Thus, the pH-mediated inhibition of eukaryotic phytoplankton may be involved in the bloom formation of N. spumigena. We also report, for the first time, the reciprocal growth inhibition of N. spumigena by diatoms resistant to alkaline conditions. As all species in this study can co-occur in the Baltic Sea during summer, these findings are highly relevant for understanding ecological interactions in planktonic communities in this and other systems experiencing regular cyanobacteria blooms.