Despite recent reductions of nutrient loading into freshwater environments, cyanobacterial harmful algal blooms (CHABS) continue to increase in frequency and magnitude, threatening global freshwater ecosystems and services. In north-temperate lakes cyanobacteria appear in early summer, succeeding green algae as the dominant phytoplankton group, a pattern thought to be mediated by changes in temperature and bioavailable nutrients. To understand additional drivers of this successional pattern our study examined the competitive interaction between Microcystis aeruginosa, a dominant contributor to CHABS, and the green alga Chlorella sorokiniana. We consider whether two factors regulate these interactions: (1) strain variation that includes the occurrence of the gene for the allelopathic toxin microcystin, and (2) host-associated bacteria. We used toxic M. aeruginosa PCC-7806, non-toxic M. aeruginosa PCC-9701, and C. sorokiniana free of all bacteria (axenic) and then re-introduced defined bacterial communities for their xenic counterparts. To model conditions of natural successional turnover, competitive interactions were accessed with reciprocal invasion experiments into steady-state populations of phytoplankton between Chlorella and either one of the Microcystis strains, with and without their associated microbiomes. Population growth was tracked using flow-cytometry, which uses intrinsic cellular properties to characterize phytoplankton and Random Forest models that distinguished between species with 99% accuracy.
Results/Conclusions
We found that M. aeruginosa strain variation, in part due to occurrence of the microcystin gene, was predictive of the competitive outcome with C. sorokiniana. Toxic M. aeruginosa, but not the non-toxic strain, invaded and proliferated in a steady-state population of C. sorokiniana. However, other phenotypic factors related to strain variation may contribute to this result. Further, we found that host-associated bacteria altered invasibility and the magnitude of competition. Invading toxic M. aeruginosa in the presence of host-associated bacteria resulted in a greater population density than in the absence of bacteria. Conversely, when M. aeruginosa was dominant, C. sorokiniana was only able to invade into the non-toxic strain, and only when grown in the absence of host-associated bacteria. Quantification of LR-microcystins (MCs) showed that invading toxic M. aeruginosa produce two-fold more MCs per cell when host-associated bacteria were absent compared to present. Our results suggest that Microcystis is a more robust competitor in the toxic strain and when host-associated bacteria are present. Host-associated bacteria might decrease the reliance on energetically costly allelochemicals, such as LR-microcystins in competition. These results expand our understanding of the key drivers of phytoplankton succession and the establishment and persistence of freshwater harmful cyanobacterial blooms.