Competitive interactions as a mechanism for chemical diversity maintenance in Nodularia spumigena

Abstract

Nodularia spumigena is a bloom-forming diazotrophic cyanobacterium inhabiting brackish waters worldwide. This species produces non-ribosomal peptides (NRPs), including the hepatotoxin nodularin, often referred to as cyanotoxin. Several known classes of NRPs have various biological activities, although their modes of action are poorly understood. In the Baltic N. spumigena, there is a high NRP chemodiversity among strains, allowing their grouping in specific chemotypes and subgroups. Therefore, it is relevant to ask whether the NRP production is affected by intraspecific interactions between the co-existing strains. Using a novel approach that combines culture technique and liquid chromatography-tandem mass spectrometry for the NRP analysis, we examined N. spumigena strains under mono- and co-culture conditions. The test strains were selected to represent N. spumigena belonging to the same or different chemotype subgroups. In this setup, we observed physiological and metabolic responses in the test strains grown without cell contact. The changes in NRP levels to co-culture conditions were conserved within a chemotype subgroup but different between the subgroups. Our results suggest that intraspecific interactions may promote a chemical diversity in N. spumigena population, with higher NRP production compared to a single-strain population. Studying allelochemical signalling in this cyanobacterium is crucial for understanding toxicity mechanisms and plankton community interactions in the Baltic Sea and other aquatic systems experiencing regular blooms.

Interspecific Interactions Drive Nonribosomal Peptide Production in Nodularia spumigena

“…Although more extracellular NODs are commonly observed due to the cell lysis ( 27 ), Hobson and Fallowfield ( 58 ) reported NOD release by intact cells. We have also observed an increase in cell-bound AP concentration and its release in the coculture of two strains of N. spumigena , belonging to different chemotype subgroups ( 11 ), which supports the potential involvement of APs in the cell‐to‐cell communication as a signaling molecule and a bioactive metabolite.…”

“…In cyanobacteria, SPUs might have multiple functions, but how their diversity is related to N. spumigena adaptability remains to be studied. Also, due to their common metabolic pathways and structural similarity, it can be speculated that different SPUs may have complementary functions as previously suggested ( 9 – 11 ). Thus, the upregulation of one SPU might compensate for downregulation of another.…”

“…Monoculture and coculture exposures were conducted in the custom-made cocultivation system (Fig. S1) ( 11 ). In brief, the system consisted of two modified glass flasks, each holding 500 mL, fitted together by a holding clamp.…”

“…S1 in the supplemental material). This system simulated a co-occurrence of these species in Pelagia and allowed us to study interspecific interactions caused by diffusible metabolites passing through the membrane without direct cell-to-cell contact ( 11 ). The monocultures were grown in the same manner as the cocultures but with the same species in both chambers.…”

Antioxidant Responses in Copepods Are Driven Primarily by Food Intake, Not by Toxin-Producing Cyanobacteria in the Diet

“…are the main contributors to these blooms. Nodularia spumigena is usually the primary concern because of the cyclic pentapeptide nodularin, a protein phosphatase inhibitor similar to microcystins ( Sivonen and Börner, 2008 ), and a broad spectrum of other metabolically active compounds ( Lage et al, 2021 ). Virtually all pelagic and benthic species are exposed to these toxic outbreaks, which often coincides with low growth and fecundity ( Koski et al, 1999 ; Engström-Öst et al, 2015 ).…”