A Ubiquitous Diatom Modulates its Microbial Consortium Through a Carrot-and-Stick Strategy

As the major primary producers in the oceans, phytoplankton excrete up to 50% of their fixed carbon into the diffusive boundary layer that surrounds individual phytoplankton cells. This region, known as the phycosphere, provides a chemically distinct and physically sheltered microenvironment from surrounding seawater. Molecules diffusing from the phycosphere enable heterotrophic bacteria to find, track and attach to phytoplankton cells to benefit from these dissolved organic excretions and in exchange supply phytoplankton cells with cofactors required for their growth. However, the mechanisms that enable ocean-drifting phytoplankton cells to attract beneficial bacteria and repel harmful ones into the phycosphere, if any, are completely unknown. To examine how phytoplankton recruit and potentially modulate their microbial consortia, we cured the ubiquitous diatom, Asterionellopsis glacialis, of its bacteria, acclimated it to bacterial absence and later reintroduced this consortium to the diatom. Within 30 minutes of reintroducing the microbial consortium, Rhodobacteraceae, a relatively minor component of the consortium, rapidly dominated the transcriptional activity of the consortium by activating uptake of diatom-secreted metabolites, suggesting these bacteria are highly attuned to the diatom phycosphere. In response to microbiome addition, the diatom restructured its transcriptional and metabolomic profiles to secrete a complex mixture of central and secondary metabolites. Addition of confirmed diatom central metabolites to bacterial isolates from the consortium coupled with transcriptional responses of the microbiome substantiated the ability of Rhodobacteraceae to access these metabolites rapidly relative to other bacteria. Surprisingly, two unique diatom secondary metabolites, azelaic acid (AzA) and rosmarinic acid (RA), promoted growth and enhanced cell attachment of Rhodobacteraceae representatives while suppressing growth and inhibiting cell attachment of opportunistic bacteria, respectively. Our results demonstrate that diatoms can modulate microbial communities in the phycosphere by releasing a suite of compounds that proliferate symbionts while suppressing opportunists.