Dissecting two contrasting phytoplankton-symbiont interaction modes based on population dynamics and gene expression patterns.

Microbial symbionts play vital roles in the health, fitness, and ecological dynamics of most eukaryotic species, making it essential to understand how host-microbe interactions shape the microbiome. Building on our previous work, we hypothesized that symbionts with diverse functions are maintained in the microbiome via a trade-off between two host-microbe interaction modes: either by better utilizing host-derived dissolved organic matter (DOM) without direct interaction with the host (unidirectional interaction) or by engaging in feedback interactions with the host that alter DOM composition to their advantage (bidirectional interaction). By screening symbionts isolated from C. sorokiniana (host), we examined growth and gene expression responses of two representative symbionts and the host. We found Curvibacter sp. thrived on spent medium from axenic C. sorokiniana with host-derived dissolved organic matter (DOM) in unidirectional interaction, whereas Falsiroseomonas sp. grew best with live C. sorokiniana cells in bidirectional interaction and exhibited a greater shift in gene expression between modes despite larger growth phase differences between treatments for Curvibacter sp. Specifically, Falsiroseomonas sp. showed differential expression of metabolic pathways that could benefit (e.g., synthesis of cofactors) or antagonize (e.g., metabolism of defensive secondary metabolites) toward the host under bidirectional interaction conditions. In response, host co-cultured with Falsiroseomonas sp. reduced its growth and triggered its higher expression of nitrogen-rich amino acid metabolism which may provide a nutritional benefit to Falsiroseomonas sp. These findings demonstrated that distinct host-microbe interaction modes drive differential symbiont strategies and play an important role in microbiome assembly. IMPORTANCE: Deciphering how host-microbe interactions shape microbiome structure is crucial for understanding host health and ecosystem function. Given the inherent complexity of host-microbe interactions, we simplified the system by separating interactions into unidirectional and bidirectional modes. Using this framework, we observed contrasting effects on the growth of two representative bacterial taxa isolated from the same host microbiome. These growth responses were further coupled with distinctive gene expression profiles in both hosts and bacteria under the different interaction modes. Together, these findings underscore the importance of considering host-microbe interaction modes in microbiome research. For example, our findings help explain how hosts can harbor functionally diverse microbial assemblages, where contrasting metabolic strategies are maintained through distinct interaction modes. Such insights are fundamental for predicting, managing, or engineering microbiomes, as well as understanding the ecological processes that drive microbiome diversity and function within host-microbiome systems in nature.