Vesicle-associated exudates from Alteromonas enhance growth and survival of Prochlorococcus in batch culture

Abstract

ABSTRACT The cyanobacterium Prochlorococcus MIT9312 requires helping functions from co-existing organisms for survival under stressful conditions. Here, we show that the helper strain Alteromonas macleodii EZ55 also facilitates greater exploitation of medium resources by Prochlorococcus. The presence of Alteromonas allowed Prochlorococcus to grow to greater cell densities, delay growth cessation, and avoid cell death relative to axenic cultures, phenotypes potentially associated with Alteromonas-driven degradation of autotoxic substances made by Prochlorococcus. We found that heat-labile high-molecular-weight Alteromonas exudates mediated the beneficial impacts on Prochlorococcus, although it is unclear which specific exudate-associated activities were responsible. Both the composition and activity of the secreted material changed after 500 generations of experimental evolution, suggesting genetic control. Some exudates were located within extracellular vesicles, which were capable of physically associating with Prochlorococcus cells and were responsible for at least some of the growth enhancement effects. Many of the functionalities observed in Alteromonas exudates (e.g., increasing phosphate availability, hydrogen peroxide degradation, and siderophore capabilities) are consistent with leaky Black Queen processes (i.e., services provided by one organism that benefit the entire community) and favor the evolution of interdependencies in microbial communities. We discuss the potential ramifications of such processes being packaged into vesicles as opposed to freely diffusing through the extracellular milieu. IMPORTANCE Heterotrophic bacteria can facilitate improved growth for numerous phytoplankton, including the highly abundant cyanobacterium Prochlorococcus. Here, we show that for the “helper” interaction between Alteromonas and Prochlorococcus, this facilitation is relevant across all phases of batch culture growth and is mediated by secreted products, including proteins and membrane vesicles. We explore the composition of these exudates and show evidence that they are altered during evolutionary adaptation in a changed environment. Heterotrophic bacteria can facilitate improved growth for numerous phytoplankton, including the highly abundant cyanobacterium Prochlorococcus. Here, we show that for the “helper” interaction between Alteromonas and Prochlorococcus, this facilitation is relevant across all phases of batch culture growth and is mediated by secreted products, including proteins and membrane vesicles. We explore the composition of these exudates and show evidence that they are altered during evolutionary adaptation in a changed environment.