Phototroph-heterotroph interactions during growth and long-term starvation across Prochlorococcus and Alteromonas diversity

Abstract

Microbial interactions such as those between phytoplankton and bacteria been studied intensively using specific model organisms, due to their potential impact on ecosystems and biogeochemistry. Yet, to what extent interactions differ between closely related organisms, or how these interactions change over time or culture conditions, remains unclear. Here, we characterize the interactions between five strains each of two globally abundant marine microorganisms, Prochlorococcus (a phototroph) and Alteromonas (a heterotroph), from the first encounter between individual strains and over more than a year of repeated cycles of exponential growth and long-term nitrogen starvation. Prochlorococcus-Alteromonas interactions had little effect on traditional growth parameters such as Prochlorococcus growth rate, maximal fluorescence or lag phase, affecting primarily the dynamics of culture decline, which we interpret as representing cell mortality and lysis. The shape of the Prochlorococcus decline curve and the carrying capacity of the co-cultures were determined by the phototroph and not the heterotroph strains involved. Comparing various mathematical models of culture mortality suggests that Prochlorococcus death rate increases over time in mono-cultures but decreases in co-cultures, with cells potentially becoming more resistant to stress. Our results demonstrate intra-species differences in ecologically-relevant co-culture outcomes. These include the recycling efficiency of N and whether the interactions are mutually synergistic or competitive. They also highlight the information-rich growth and death curves as a useful readout of the interaction phenotype. Significance StatementInteractions between phytoplankton and marine bacteria impact global ecosystems and biogeochemistry. Here, we explore how intra-species variability affects the interactions between Prochlorococcus, a globally abundant photosynthetic cyanobacetrium and Alteromonas, a heterotrophic bacterium that lives off and recycles organic matter. Under nitrogen starvation, Prochlorococcus growing alone increasingly accumulate damage and die, whereas in co-culture with Alteromonas they become increasingly resilient. The specific Prochlorococcus strain had a much larger effect on co-culture behavior than the Alteromonas strain, determining whether the interactions are mutually synergistic or potentially competitive. These results show how ecologically relevant outcomes of interactions may vary between closely related microorganisms, and highlight growth and death curves from laboratory (co)-cultures as information-rich views of microbial growth and death.