The mechanism of bacterial colonization of phytoplankton phycospheres

Abstract

Interactions between phytoplankton and bacteria play major roles in global biogeochemical cycles and oceanic nutrient fluxes. These interactions occur in the immediate microenvironment surrounding phytoplankton cells, known as the phycosphere. The phycosphere, akin to the rhizosphere in terrestrial plants, serves as a critical interface for microbial interactions, influenced by the diffusion of organic compounds from phytoplankton. This thesis examines the intricate dynamics of phytoplankton-bacteria interactions within the phycosphere, focusing on the mechanism of bacterial colonization. Through a comprehensive exploration encompassing in vitro studies, environmental sampling, and advanced genomic and metabolomic analyses, this work sheds light on the mechanisms underlying the colonization of the phycosphere by specific bacterial taxa. Chapter II of the thesis highlights Roseobacteraceae, specifically Sulfitobacter spp. as key players in the assembly of phytoplankton microbiomes and demonstrates that the early stages of colonization include selection by the host and interspecies associations. Chapter III investigates the family Roseobacteraceae in an environmental context and tracks microbial community changes in response to phytoplankton bloom dynamics. It uncovers that specific Roseobacteraceae members possess unique genetic determinants (tad genes) that likely facilitate their attachment to host cells, suggesting a niche differentiation within this important group of bacteria. Chapter IV confirms the involvement of tad genes in the colonization of the phycosphere of the diatom Asterionellopsis glacialis by Roseobacteraceae through co-culture experiments and transcriptomics. Chapter V looks at phycosphere colonization from the vantage point of the phytoplankton host. It identifies the host-derived secondary metabolites, azelaic acid and rosmarinic acid that significantly influence the attachment and motility of symbiotic Roseobacteraceae and opportunistic Alteromonadaceae to modulate the microbiome. Collectively, this thesis proposes a holistic theory of phycosphere colonization that integrates microbial network structuring, niche differentiation, and host filtering. This theory challenges existing paradigms by highlighting synergy rather than competition of stochastic and deterministic processes during colonization. This thesis advances our understanding of phytoplankton-bacteria interactions by illustrating how specific bacterial taxa are selected by phytoplankton not merely to meet nutritional demands but to modulate the microbiome through competition and symbiosis and further unravels the mechanism of host effects in shaping their microbiomes.