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Labile Dissolved Organic Matter Compound Characteristics Select for Divergence in Marine Bacterial Activity and Transcription
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Lnuc EEMiS)ORCID iD: 0000-0003-4787-7021
Univ Vigo, Spain.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Linnaeus University, Linnaeus Knowledge Environments, Water. (Lnuc EEMiS)ORCID iD: 0000-0002-8779-6464
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Linnaeus University, Linnaeus Knowledge Environments, Water. (Lnuc EEMiS)ORCID iD: 0000-0002-6405-1347
2020 (English)In: Frontiers in Microbiology, E-ISSN 1664-302X, Vol. 11, p. 1-19, article id 588778Article in journal (Refereed) Published
Abstract [en]

Bacteria play a key role in the planetary carbon cycle partly because they rapidly assimilate labile dissolved organic matter (DOM) in the ocean. However, knowledge of the molecular mechanisms at work when bacterioplankton metabolize distinct components of the DOM pool is still limited. We, therefore, conducted seawater culture enrichment experiments with ecologically relevant DOM, combining both polymer and monomer model compounds for distinct compound classes. This included carbohydrates (polysaccharides vs. monosaccharides), proteins (polypeptides vs. amino acids), and nucleic acids (DNA vs. nucleotides). We noted pronounced changes in bacterial growth, activity, and transcription related to DOM characteristics. Transcriptional responses differed between compound classes, with distinct gene sets ("core genes") distinguishing carbohydrates, proteins, and nucleic acids. Moreover, we found a strong divergence in functional transcription at the level of particular monomers and polymers (i.e., the condensation state), primarily in the carbohydrates and protein compound classes. These specific responses included a variety of cellular and metabolic processes that were mediated by distinct bacterial taxa, suggesting pronounced functional partitioning of organic matter. Collectively, our findings show that two important facets of DOM, compound class and condensation state, shape bacterial gene expression, and ultimately select for distinct bacterial (functional) groups. This emphasizes the interdependency of marine bacteria and labile carbon compounds for regulating the transformation of DOM in surface waters.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2020. Vol. 11, p. 1-19, article id 588778
Keywords [en]
labile DOM compounds, carbohydrates, nucleic acids, proteins, bacterial metatranscriptomics, microcosms, brackish water system, functional partitioning
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-98814DOI: 10.3389/fmicb.2020.588778ISI: 000578814700001PubMedID: 33101262Scopus ID: 2-s2.0-85092392878OAI: oai:DiVA.org:lnu-98814DiVA, id: diva2:1500264
Available from: 2020-11-11 Created: 2020-11-11 Last updated: 2025-09-23Bibliographically 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)
Opponent
Supervisors
Available from: 2021-04-19 Created: 2021-04-16 Last updated: 2025-09-23Bibliographically approved

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Pontiller, BenjaminLundin, DanielPinhassi, Jarone

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