Nutrient-dependent interactions between a marine copiotroph Alteromonas and a diatom Thalassiosira pseudonana

Abstract

ABSTRACT Bacteria-diatom interactions in the ocean are diverse but usually studied in static conditions, which limits our understanding of their importance in marine ecosystems and biogeochemical cycles. Here, we explored the dynamic interactions between an ubiquitous marine bacterium Alteromonas sp. and a diatom Thalassiosira pseudonana under different nutrient conditions. In oligotrophic conditions, minor shifts in nutrients qualitatively altered the interactions from mutualism during early exponential growth to weak parasitism during the late stationary phase. Organic matter-activated Alteromonas chemotactically swam toward, attached on, and dramatically broke down T. pseudonana cells, leading to an aggressive parasitic behavior with a 95% algicidal rate. Meanwhile, inorganic matter-activated T. pseudonana showed amensalism against Alteromonas , resulting in an ephemeral decrease of bacterial abundance by 27%. Interestingly, when both organics and inorganics were sufficient, Alteromonas suppressed diatom growth by inhibiting the cell division, while the surviving T. pseudonana restored proliferation with a significantly smaller cell size inconducive to bacterial attachment, demonstrating an intense competition. The results further indicated that the algicidal effect of Alteromonas was controlled by the cell-specific protease activity and the number of attached bacteria on the diatom cell surface, both of which were related to nutrient conditions. Since the nature and intensity of bacteria-diatom interaction depend on the composition and richness of nutrients, it mechanistically explains the tripartite relationship among bacterial proliferation, nutrient viability, and algal demise during blooms. The algicidal behavior of copiotrophs also potentially enhances the contribution of a microbial carbon pump to carbon sequestration in the ocean. IMPORTANCE As the major producers and consumers, phytoplankton and bacteria play central roles in marine ecosystems and their interactions show great ecological significance. Whether mutualistic or antagonistic, the interaction between certain phytoplankton and bacterial species is usually seen as a derivative of intrinsic physiological properties and rarely changes. This study demonstrated that the interactions between the ubiquitously co-occurring bacteria and diatom, Alteromonas and Thalassiosira pseudonana , varied with nutrient conditions. They overcame hardship together in oligotrophic seawater but showed antagonistic effects against each other under nutrient amendment. The contact-dependent algicidal behavior of Alteromonas based on protease activity solved the paradox among bacterial proliferation, nutrient viability, and algal demise haunting other known non-contact-dependent algicidal processes and might actually trigger the collapse of algal blooms in situ . The chemotactic and swarming movement of Alteromonas might also contribute greatly to the breakdown of “marine snow,” which could redirect the carbon sequestration pathway in the ocean.