Diatom modulation of select bacteria through use of two unique secondary metabolites
Type
ArticleAuthors
Shibl, Ahmed A.
Isaac, Ashley

Ochsenkühn, Michael A.

Cardenas, Anny
Fei, Cong
Behringer, Gregory
Arnoux, Marc

Drou, Nizar
Santos, Miraflor P.
Gunsalus, Kristin C.

Voolstra, Christian R.

Amin, Shady A.

KAUST Department
Red Sea Research Center (RSRC)Biological and Environmental Sciences and Engineering (BESE) Division
Date
2020-10-16Online Publication Date
2020-10-16Print Publication Date
2020-11-03Submitted Date
2020-06-12Permanent link to this record
http://hdl.handle.net/10754/665607
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Show full item recordAbstract
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.Citation
Shibl, A. A., Isaac, A., Ochsenkühn, M. A., Cárdenas, A., Fei, C., Behringer, G., … Amin, S. A. (2020). Diatom modulation of select bacteria through use of two unique secondary metabolites. Proceedings of the National Academy of Sciences, 202012088. doi:10.1073/pnas.2012088117Sponsors
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.Additional Links
http://www.pnas.org/lookup/doi/10.1073/pnas.2012088117ae974a485f413a2113503eed53cd6c53
10.1073/pnas.2012088117
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