An algicidal bacterium shapes the microbiome during outdoor diatom cultivation collapse

Biogeochemistry and productivity of algae-dominated environments is fundamentally influenced by the diversity and activity of bacteria. Namely, algicidal bacteria that prey on algal hosts can control elemental cycling and host populations within outdoor algal ponds used for biofuel production. In this study, we describe the genomic and proteomic signatures of a putative algicidal bacterium, Kordia sp. (family Flavobacteriaceae), that bloomed during a population-wide crash of the biofuel diatom, Phaeodactylum tricornutum. This Kordia sp. bloom occurred after 29 days of cultivation in outdoor algal raceway ponds inoculated with P. tricornutum, but not in parallel ponds inoculated with Microchloropsis salina. Several signatures of antagonism expressed by Kordia during diatom demise highlights previously unexplored mechanisms that may aid in algicidal activity or bacterial competition, including the type VI secretion system and hydrogen peroxide production. Analysis of accompanying downstream microbiota (primarily of the Rhodobacteraceae family) provides evidence that cross-feeding is important in supporting microbial diversity during algal demise. Specifically, in situ and laboratory data suggest that Kordia acts as a primary degrader of biopolymers during algal demise, and co-occurring Rhodobacteraceae exploit degradation molecules or scavenge metabolic byproducts for carbon. Further, targeted analysis of 30 Rhodobacteraceae metagenome assembled genomes suggest algal pond Rhodobacteraceae commonly harbor pathways for carbon monoxide oxidation, a potential strategy to persist under competition. Collectively, these observations further constrain the role of algicidal bacteria in the aquatic ecosystem.