Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may tune microbial communities and employed an integrated multiomics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is numerically rare but globally distributed in the world’s oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.
|Original language||English (US)|
|Journal||Proceedings of the National Academy of Sciences|
|State||Published - Oct 17 2020|
Bibliographical noteKAUST Repository Item: Exported on 2020-10-19
Acknowledgements: We thank the NYU Abu Dhabi Core Technology Platforms for support in genomics sequencing and mass spectrometry. We also thank Dain McParland for help collecting water samples and Bryndan P.Durham and Elodie Ghedin for helpful comments on the manuscript. This project was supported by a grant from the NYU Abu Dhabi Research institute to K.C.G. (ADHPG-CGSB1) and grants from NYU Abu Dhabi (AD179) and NOAA (#NA19NOS4780183) to S.A.A.