Marine phototroph-heterotroph interactions

The productivity of marine systems relies on the growth of phytoplankton (phototrophs) which are mainly limited by nutrient availability. Bacteria benefit from the organic matter released by the phototrophs, re-mineralising the scarce nutrients within the system and making them available again to the phytoplankton (Christie-Oleza et al., 2017b). Nevertheless, other positive phototroph-heterotroph interactions have been described (i.e. the Black Queen Hypothesis) in Morris et al. (2012) based on vitamin exchange and alleviation of oxidative stress. Negative interactions such as competition for limited nutrients have also been reported (Thingstad et al., 1993) which is represented by the Red Queen Hypothesis as an evolutionary race. Here, nine phototrophs and 14 heterotrophs were co-cultivated in one-to-one species combinations with the aim of detecting a general behaviour of interactions between marine microbes. The interaction established in each co-culture was characterised based on population abundance and time of survival in both natural oligotrophic (SW) and nutrient-enriched seawater (ESW), compared to mono-culture conditions. Four different types of interactions (i.e. positive, semi-positive, neutral and negative) were detected in the 126 co-culture combinations. Many interactions varied between nutrient conditions highlighting nutrient availability as a key player in establishing interactions, as well as the need to test microorganisms in natural SW to reach reliable conclusions. In order to deepen our understanding of phototroph-heterotroph interactions, the proteomic profile of the co-cultures of the model heterotroph R. pomeroyi with each one of the nine phototrophs was performed in SW conditions. In the presence of the phototrophs, R. pomeroyi showed generic responses (e.g. in amino-acid uptake and N- metabolism, urea metabolism, vitamin biosynthesis and scavenging for aromatic compounds and CO metabolism as energy sources) but also species-specific responses (e.g. the relief of P stress, the reduction of specific S compounds and oxidative stress responses). In return, the nine phototrophs reacted differently to the presence of R. pomeroyi, with some phototrophs relying on R. pomeroyi for key metabolic processes and reaching some level of metabolic coupling with the heterotroph. The magnitude of species-specificity in the interactions between phototrophs and heterotrophs in natural seawater demonstrates the complexity of the system and the usefulness of this data for the interpretation of global biogeochemical cycles