Diatom modulation of select bacteria through use of two unique secondary metabolites
| Autor: | Michael A. Ochsenkühn, Kristin C. Gunsalus, Miraflor P. Santos, Ahmed A. Shibl, Ashley Isaac, Gregory Behringer, Shady A. Amin, Cong Fei, Marc Arnoux, Christian R. Voolstra, Anny Cárdenas, Nizar Drou |
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| Rok vydání: | 2020 |
| Předmět: |
Azelaic acid
Oceans and Seas Bacterial growth Depsides Microbiology 03 medical and health sciences chemistry.chemical_compound microbiomes ddc:570 medicine Animals Metabolomics phytoplankton–bacteria interactions Dicarboxylic Acids Secretion Microbiome Secondary metabolism 030304 developmental biology Diatoms secondary metabolism 0303 health sciences phycosphere Multidisciplinary Bacteria Ecology biology 030306 microbiology Gene Expression Profiling Microbiota Rosmarinic acid fungi Biological Sciences biology.organism_classification Diatom chemistry Cinnamates Phytoplankton Metagenome Metagenomics Water Microbiology medicine.drug |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America |
| ISSN: | 1091-6490 0027-8424 |
| DOI: | 10.1073/pnas.2012088117 |
| Popis: | Significance Phytoplankton are major primary producers in the marine environment that excrete a wide range of metabolites. These exudates support the growth of surrounding bacteria that in turn provide phytoplankton cells with resources and growth cofactors to proliferate. Unlike multicellular eukaryotes with dedicated structures housing microbiomes, mechanisms enabling unicellular eukaryotic phytoplankton hosts to modulate potential symbionts and opportunists within a natural microbial community are unknown. Exposure of a host phytoplankton cell to its natural microbial community triggers major transcriptional and metabolic reprogramming to release unique secondary metabolites that selectively enable growth and attachment of symbiotic taxa while simultaneously suppressing the colonization of nonsymbiont bacteria. These results suggest strong and highly selective microbiome-modulating strategies shared across the unicellular and multicellular eukaryotic lineages. 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. |
| Databáze: | OpenAIRE |
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