Enzymatically active exudates from Alteromonas facilitate Prochlorococcus survival in stationary phase

Abstract

The cyanobacterium Prochlorococcus has a conspicuously reduced genome causing it to require help from co-existing organisms for survival under a variety of stressful conditions. In this work we demonstrated that the heterotrophic bacterium Alteromonas macleodii EZ55 facilitated the survival of Prochlorococcus MIT9312 batch co-cultures as they entered stationary phase. We further showed that exudates from both Alteromonas and Prochlorococcus were responsible for this effect. Unidentified toxic exudates of Prochlorococcus lowered the carrying capacity of Pro99 medium for axenic Prochlorococcus cells, whereas heat-labile high-molecular weight exudates of Alteromonas both removed the effect of Prochlorococcus exudates and extended the lifespan of axenic Prochlorococcus cultures. Alteromonas exudates contained a wide variety of proteins and demonstrated enzymatic activities. Some of these proteins and activities may have been packaged within extracellular membrane vesicles, which we identified within Alteromonas exudates and found capable of physically associating with Prochlorococcus cells. Many of the functionalities observed in Alteromonas exudates (e.g., increasing phosphate availability, degrading hydrogen peroxide) were consistent with leaky Black Queen processes, which are defined as services provided by one organism that benefit the entire community and favor the evolution of interdependencies in microbial communities. Therefore, we discuss the potential ramifications of such processes being packaged into vesicles as opposed to freely diffusing through the extracellular milieu.