The genetic and ecophysiological diversity of Microcystis.

Microcystis is a cyanobacterium that forms toxic blooms in freshwater ecosystems around the world. Biological variation among taxa within the genus is apparent through genetic and phenotypic differences between strains and via the spatial and temporal distribution of strains in the environment, and this fine-scale diversity exerts strong influence over bloom toxicity. Yet we do not know how varying traits of Microcystis strains govern their environmental distribution, the tradeoffs and links between these traits, or how they are encoded at the genomic level. Here we synthesize current knowledge on the importance of diversity within Microcystis and on the genes and traits that likely underpin ecological differentiation of taxa. We briefly review spatial and environmental patterns of Microcystis diversity in the field and genetic evidence for cohesive groups within Microcystis. We then compile data on strain-level diversity regarding growth responses to environmental conditions and explore evidence for variation of community interactions across Microcystis strains. Potential links and tradeoffs between traits are identified and discussed. The resulting picture, while incomplete, highlights key knowledge gaps that need to be filled to enable new models for predicting strain-level dynamics, which influence the development, toxicity and cosmopolitan nature of Microcystis blooms.

Host specificity of microbiome assembly and its fitness effects in phytoplankton.

Insights into symbiosis between eukaryotic hosts and their microbiomes have shifted paradigms on what determines host fitness, ecology, and behavior. Questions remain regarding the roles of host versus environment in shaping microbiomes, and how microbiome composition affects host fitness. Using a model system in ecology, phytoplankton, we tested whether microbiomes are host-specific, confer fitness benefits that are host-specific, and remain conserved in time in their composition and fitness effects. We used an experimental approach in which hosts were cleaned of bacteria and then exposed to bacterial communities from natural environments to permit recruitment of microbiomes. We found that phytoplankton microbiomes consisted of a subset of taxa recruited from these natural environments. Microbiome recruitment was host-specific, with host species explaining more variation in microbiome composition than environment. While microbiome composition shifted and then stabilized over time, host specificity remained for dozens of generations. Microbiomes increased host fitness, but these fitness effects were host-specific for only two of the five species. The shifts in microbiome composition over time amplified fitness benefits to the hosts. Overall, this work solidifies the importance of host factors in shaping microbiomes and elucidates the temporal dynamics of microbiome compositional and fitness effects.

Microbiomes Reduce Their Host's Sensitivity to Interspecific Interactions.

Bacteria associated with eukaryotic hosts can affect host fitness and trophic interactions between eukaryotes, but the extent to which bacteria influence the eukaryotic species interactions within trophic levels that modulate biodiversity and species coexistence is mostly unknown. Here, we used phytoplankton, which are a classic model for evaluating interactions between species, grown with and without associated bacteria to test whether the bacteria alter the strength and type of species interactions within a trophic level. We demonstrate that host-associated bacteria alter host growth rates and carrying capacity. This did not change the type but frequently changed the strength of host interspecific interactions by facilitating host growth in the presence of an established species. These findings indicate that microbiomes can regulate their host species' interspecific interactions. As between-species interaction strength impacts their ability to coexist, our findings show that microbiomes have the potential to modulate eukaryotic species diversity and community composition.IMPORTANCE Description of the Earth's microbiota has recently undergone a phenomenal expansion that has challenged basic assumptions in many areas of biology, including hominid evolution, human gastrointestinal and neurodevelopmental disorders, and plant adaptation to climate change. By using the classic model system of freshwater phytoplankton that has been drawn upon for numerous foundational theories in ecology, we show that microbiomes, by facilitating their host population, can also influence between-species interactions among their eukaryotic hosts. Between-species interactions, including competition for resources, has been a central tenet in the field of ecology because of its implications for the diversity and composition of communities and how this in turn shapes ecosystem functioning.

Genotype and host microbiome alter competitive interactions between Microcystis aeruginosa and Chlorella sorokiniana.

Cyanobacterial harmful algal blooms (cyanoHABs) 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 used reciprocal invasion experiments to examine the competitive interaction between Microcystis aeruginosa, a dominant contributor to cyanoHABs, and the green alga Chlorella sorokiniana. We considered two factors that may impact these interactions: (1) strain variation, with a specific emphasis on the presence or absence of the gene for the hepatotoxin microcystin, and (2) host-associated bacteria. We used toxic M. aeruginosa PCC 7806 (microcystin producing strain), a non-toxic mutant of PCC 7806, non-toxic M. aeruginosa PCC 9701 (non-microcystin producing strain), and C. sorokiniana. Each organism was available free of all bacteria (i.e., axenic) and with a re-introduced defined bacterial community to generate their xenic counterparts. Competitive interactions were assessed with reciprocal invasion experiments between paired xenic and paired axenic populations of C. sorokiniana and one of the two Microcystis strains, each assessed separately. Flow cytometry and random forest models were used to rapidly discriminate and quantify phytoplankton population densities with 99% accuracy. We found that M. aeruginosa PCC 7806, but not strain PCC 9701, could proliferate from low abundance in a steady-state population of C. sorokiniana. Further, the presence of bacteria allowed M. aeruginosa PCC 7806 to grow to a higher population density into an established C. sorokiniana population than when grown axenic. Conversely, when M. aeruginosa was dominant, C. sorokiniana was only able to proliferate from low density into the PCC 9701 strain, and only when axenic. The mutant of PCC 7806 lacking the ability to produce microcystin behaved similarly to the toxic wild-type, implying microcystin is not responsible for the difference in competitive abilities observed between the two wild-type strains. Quantification of microcystins (MCs) when PCC 7806 M. aeruginosa was introduced into the C. sorokiniana culture showed two-fold more MCs per cell when host-associated bacteria were absent compared to present in both species cultures. Our results show that the ability of M. aeruginosa to compete with C. sorokiniana is determined by genomic differences beyond genes involved in microcystin toxin generation and indicate an important role of host-associated bacteria in mediating phytoplankton interspecies interactions. These results expand our understanding of the key drivers of phytoplankton succession and the establishment and persistence of freshwater harmful cyanobacterial blooms.