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Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. GEOMAR Helmholtz Ctr Ocean Res Kiel, Germany. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0003-4787-7021
Universidadde de Vigo, Spain.
Universidadde de Vigo, Spain.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0002-2747-6346
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2022 (English)In: The ISME Journal, ISSN 1751-7362, E-ISSN 1751-7370, Vol. 16, p. 2360-2372Article in journal (Refereed) Published
Abstract [en]

Coastal upwelling zones are veritable hotspots of oceanic productivity, driven by phytoplankton photosynthesis. Bacteria, in turn, grow on and are the principal remineralizers of dissolved organic matter (DOM) produced in aquatic ecosystems. However, knowledge of the molecular processes that key bacterial taxa employ to regulate the turnover of phytoplankton-derived DOM has yet to advance. We therefore carried out a comparative metatranscriptomics analysis with parallel sampling of bacterioplankton during experimental and natural phytoplankton blooms in the Northwest Iberian upwelling system. The experiment analysis uncovered a taxon-specific progression of transcriptional responses from bloom development, over early decay, to senescence phases. This included pronounced order-specific differences in regulation of glycoside hydrolases and peptidases along with transporters, supporting the notion that functional resource partitioning is dynamically structured by temporal changes in available DOM. In addition, comparative analysis of experiment and field blooms revealed a large degree of metabolic plasticity in the degradation and uptake of carbohydrates and nitrogen-rich compounds, suggesting these gene systems critically contribute to modulating the stoichiometry of the coastal DOM pool. Collectively, our findings suggest that cascades of transcriptional responses in gene systems for the utilization of organic matter and nutrients largely shape the fate of organic matter on the short time scales typical of upwelling-driven phytoplankton blooms.

Place, publisher, year, edition, pages
Nature Publishing Group, 2022. Vol. 16, p. 2360-2372
Keywords [en]
Marine bacteria, metatranscriptomics, labile dissolved organic carbon, resource partitioning, microbial ecology, succession, traits, ecophysiology
National Category
Biological Sciences Microbiology Ecology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-102049DOI: 10.1038/s41396-022-01273-0ISI: 000822288300001PubMedID: 35804052Scopus ID: 2-s2.0-85133605379OAI: oai:DiVA.org:lnu-102049DiVA, id: diva2:1543016
Funder
Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning
Note

Is included in the dissertation as a manuscript titled: Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system

Available from: 2021-04-09 Created: 2021-04-09 Last updated: 2023-02-21Bibliographically approved
In thesis
1. Molecular mechanisms involved in prokaryotic cycling of labile dissolved organic matter in the sea
Open this publication in new window or tab >>Molecular mechanisms involved in prokaryotic cycling of labile dissolved organic matter in the sea
2021 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Roughly half of the global primary production originates from microscopic phytoplankton in marine ecosystems, converting carbon dioxide into organic matter. This organic matter pool consists of a myriad of compounds that fuel heterotrophic bacterioplankton. However, knowledge of the molecular mechanisms – particularly the metabolic pathways involved in the degradation and utilization of dissolved organic matter (DOM) – and transcriptional dynamics over spatiotemporal gradients are still scarce. Therefore, we studied the molecular mechanisms of bacterioplankton communities, including archaea, involved in the cycling of DOM, over different spatiotemporal scales in experiments and through field observations.

In seawater experiments, we found a divergence of bacterioplankton transcriptional responses to different organic matter compound classes (carbohydrates, nucleic acids, and proteins) and condensation states (monomers or polymers). These responses were associated with distinct bacterial taxa, suggesting pronounced functional partitioning of these compounds in the Sea. Baltic Proper mesocosms amended with two different river loadings (forest versus agriculture river water) revealed a divergence in gene expression patterns between treatments during bloom decay. This was particularly true for genes in phosphorus and nitrogen metabolism, highlighting the importance and sensitivity of interaction effects between river- and phytoplankton-derived DOM in regulating bacterial activity responses to changes in precipitation-induced riverine runoff.

In shipboard mesocosms in an Atlantic coastal upwelling system, we found significant changes in bacterioplankton transcription of hydrolyzing enzymes and membrane transporters from phytoplankton bloom development to senescence, primarily driven by phytoplankton-derived DOM and dissolved organic carbon dynamics. These responses differed substantially between bacterial orders, suggesting that functional resource partitioning is dynamically structured by temporal changes in DOM quantity and quality. Further analysis of these gene systems in a stratified fjord revealed pronounced divergence in transcription with depth and between bacterial taxa; moreover, transcription was more variable in the surface waters. This highlights the interplay between functional and physical partitioning of biogeochemical cycles. Collectively, the findings in this thesis contribute novel insights into the interdependency between prokaryotes and DOM by shedding light on the mechanisms involved in DOM cycling over ecologically relevant spatiotemporal scales.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2021. p. 90
Series
Linnaeus University Dissertations ; 412/2021
Keywords
Bacteria and archaea, labile dissolved organic matter, metatranscriptomics, monomers, polymers, carbohydrate-active enzymes (CAZymes), peptidases, membrane transporters
National Category
Biological Sciences Natural Sciences Ecology Microbiology
Research subject
Natural Science; Ecology, Aquatic Ecology; Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-102053 (URN)978-91-89283-66-4 (ISBN)978-91-89283-65-7 (ISBN)
Public defence
2021-05-12, Fulriggaren, Kalmar, 13:00 (English)
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Supervisors
Available from: 2021-04-19 Created: 2021-04-16 Last updated: 2024-03-05Bibliographically approved

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Pontiller, BenjaminAmnebrink, DennisPérez Martínez, ClaraLundin, DanielPinhassi, Jarone

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