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Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
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2014 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 111, no 35, p. E3650-E3658Article in journal (Refereed) Published
Abstract [en]

Proteorhodopsin (PR) is present in half of surface ocean bacterioplankton, where its light-driven proton pumping provides energy to cells. Indeed, PR promotes growth or survival in different bacteria. However, the metabolic pathways mediating the light responses remain unknown. We analyzed growth of the PR-containing Dokdonia sp. MED134 (where light-stimulated growth had been found) in seawater with low concentrations of mixed [yeast extract and peptone (YEP)] or single (alanine, Ala) carbon compounds as models for rich and poor environments. We discovered changes in gene expression revealing a tightly regulated shift in central metabolic pathways between light and dark conditions. Bacteria showed relatively stronger light responses in Ala compared with YEP. Notably, carbon acquisition pathways shifted toward anaplerotic CO2 fixation in the light, contributing 31 +/- 8% and 24 +/- 6% of the carbon incorporated into biomass in Ala and YEP, respectively. Thus, MED134 was a facultative double mixotroph, i.e., photo- and chemotrophic for its energy source and using both bicarbonate and organic matter as carbon sources. Unexpectedly, relative expression of the glyoxylate shunt genes (isocitrate lyase and malate synthase) was >300-fold higher in the light-but only in Ala-contributing a more efficient use of carbon from organic compounds. We explored these findings in metagenomes and metatranscriptomes and observed similar prevalence of the glyoxylate shunt compared with PR genes and highest expression of the isocitrate lyase gene coinciding with highest solar irradiance. Thus, regulatory interactions between dissolved organic carbon quality and central metabolic pathways critically determine the fitness of surface ocean bacteria engaging in PR phototrophy.

Place, publisher, year, edition, pages
2014. Vol. 111, no 35, p. E3650-E3658
National Category
Ecology
Research subject
Natural Science, Aquatic Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-37306DOI: 10.1073/pnas.1402617111ISI: 000341230800012Scopus ID: 2-s2.0-84907227908OAI: oai:DiVA.org:lnu-37306DiVA, id: diva2:750247
Available from: 2014-09-27 Created: 2014-09-27 Last updated: 2017-12-11Bibliographically approved
In thesis
1. Bacterioplankton in the light of seasonality and environmental drivers
Open this publication in new window or tab >>Bacterioplankton in the light of seasonality and environmental drivers
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Bacterioplankton are keystone organisms in marine ecosystems. They are important for element cycles, by transforming dissolved organic carbon and other nutrients. Bacterioplankton community composition and productivity rates change in surface waters over spatial and temporal scales. Yet, many underlying biological processes determining when, why and how bacterioplankton react to changes in environmental conditions are poorly understood. Here, I used experiments with model bacteria and natural assemblages as well as field studies to determine molecular, physiological and ecological responses allowing marine bacteria to adapt to their environment.

Experiments with the flavobacterium Dokdonia sp. MED134 aimed to determine how the metabolism of bacteria is influenced by light and different organic matter. Under light exposure, Dokdonia sp. MED134 expressed proteorhodopsin and adjusted its metabolism to use resources more efficiently when growing with lower-quality organic matter. Similar expression patterns were found in oceanic datasets, implying a global importance of photoheterotrophic metabolisms for the ecology of bacterioplankton.

Further, I investigated how the composition and physiology of bacterial assemblages are affected by elevated CO2 concentrations and inorganic nutrients. In a large-scale experiment, bacterioplankton could keep productivity and community structure unaltered by adapting the gene expression under CO2 stress. To maintain pH homeostasis, bacteria induced higher expression of genes related to respiration, membrane transport and light acquisition under low-nutrient conditions. Under high-nutrient conditions with phytoplankton blooms, such regulatory mechanisms were not necessary. These findings indicate that open ocean systems are more vulnerable to ocean acidification than coastal waters.

Lastly, I used field studies to resolve how bacterioplankton is influenced by environmental changes, and how this leads to seasonal succession of marine bacteria. Using high frequency sampling over three years, we uncovered notable variability both between and within years in several biological features that rapidly changed over short time scales. These included potential phytoplankton-bacteria linkages, substrate uptake rates, and shifts in bacterial community structure. Thus, high resolution time series can provide important insights into the mechanisms controlling microbial communities.

Overall, this thesis highlights the advantages of combining molecular and traditional oceanographic methodological approaches to study ecosystems at high resolution for improving our understanding of the physiology and ecology of microbial communities and, ultimately, how they influence biogeochemical processes.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2017. p. 62
Series
Linnaeus University Dissertations ; 303/2017
Keywords
marine bacteria, marine microbiology, seasonal succession, ocean acidification, proteorhodopsin, photoheterotrophy, microbial time series
National Category
Environmental Sciences Oceanography, Hydrology and Water Resources Microbiology
Research subject
Ecology, Aquatic Ecology; Ecology, Microbiology; Natural Science, Environmental Science
Identifiers
urn:nbn:se:lnu:diva-69130 (URN)978-91-88761-03-3 (ISBN)978-91-88761-02-6 (ISBN)
Public defence
2018-01-12, Fullriggaren, Sjöfartshögskolan, Kalmar, 09:30 (English)
Supervisors
Funder
Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGESwedish Research Council
Available from: 2017-12-11 Created: 2017-12-11 Last updated: 2018-02-21Bibliographically approved

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Palovaara, JoakimAkram, NeelamBaltar, FedericoBunse, CarinaPinhassi, Jarone

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