Marine phytoplankton and heterotrophic bacteria rapidly adapt to future pCO2conditions in experimental co-cultures

Abstract

ABSTRACTThe CO2content of Earth’s atmosphere is rapidly increasing due to human consumption of fossil fuels. Models based on short-term culture experiments predict that major changes will occur in marine phytoplankton communities in the future ocean, but these models rarely consider how the evolutionary potential of phytoplankton or interactions within marine microbial communities may influence these changes. Here we experimentally evolved representatives of four phytoplankton functional types (silicifiers, calcifiers, coastal cyanobacteria, and oligotrophic cyanobacteria) in co-culture with a heterotrophic bacterium,Alteromonas, under either present-day or predicted future pCO2conditions. Growth rates of cyanobacteria generally increased under both conditions, and the growth defects observed in ancestralProchlorococcuscultures at elevated pCO2and in axenic culture were diminished after evolution, possibly due to regulatory mutations in antioxidant genes. Except forProchlorococcus, mutational profiles suggested phytoplankton experienced primarily purifying selection, but mostAlteromonaslineages showed evidence of directional selection, especially when co-cultured with eukaryotic phytoplankton, where evolution appeared to favor a broad metabolic switch from growth on small organic acids to catabolism of more complex carbon substrates. EvolvedAlteromonaswere also poorer “helpers” forProchlorococcus, supporting the assertion that the interaction betweenProchlorococcusand heterotrophic bacteria is not a true mutualism but rather a competitive interaction stabilized by Black Queen processes. This work provides new insights on how phytoplankton will respond to anthropogenic change and on the evolutionary mechanisms governing the structure and function of marine microbial communities.