Coevolution of marine phytoplankton and Alteromonas bacteria in response to pCO2 and co-culture

As a result of human activity, Earth’s atmosphere and climate are changing at an unprecedented pace. Models based on short-term experiments predict major changes will occur in marine phytoplankton communities in the future ocean, but rarely consider how evolution or interactions with other microbes may influence these changes. Here we experimentally evolved several phytoplankton in co-culture with a heterotrophic bacterium, Alteromonas sp. EZ55, under either present-day or predicted future pCO2 conditions. Growth rates of phytoplankton generally increased over time under both conditions, but only Thalassiosira oceanica had evidence of a growth rate trade-off in the ancestral environment after evolution at elevated pCO2. The growth defects observed in ancestral Prochlorococcus cultures at elevated pCO2 and in axenic culture were diminished after evolution, possibly due to regulatory mutations in antioxidant genes. Except for Prochlorococcus, mutational profiles suggested phytoplankton experienced primarily purifying selection, but most Alteromonas lineages showed evidence of directional selection, where evolution appeared to favor a metabolic switch between growth on small organic acids with cyanobacteria versus catabolism of more complex carbon substrates with eukaryotic phytoplankton. Evolved Alteromonas were also poorer “helpers” for Prochlorococcus, consistent with that interaction being a competitive Black Queen process rather than a true mutualism. This work provides new insights on how phytoplankton will respond to increased pCO2 and on the evolutionary mechanisms governing phytoplankton:bacteria interactions. It also clearly demonstrates that both evolution and interspecies interactions must be considered to predict future marine biogeochemistry.