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  • 1.
    Akram, Neelam
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    From genes to ecological function in marine bacteria2013Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Bacteria in the sea are constantly exposed to environmental challenges (e.g. variations in nutrient concentrations, temperature and light conditions), and therefore appropriate gene expression response strategies to cope with them efficiently are evolved. This thesis investigates some interconnected questions regarding such adaptive strategies employed by marine bacteria.

    The recently discovered ability of bacteria to use the membrane protein proteorhodopsin (PR) to harvest light energy for cell metabolism were investigated in Vibrio sp. AND4 and Dokdonia sp. MED134. PR phototrophy in AND4 promoted survival during starvation, the molecular basis for which were the upregulation of the PR gene by nutrient limitation rather than light. MED134, in contrast, uses PR phototrophy to grow better, and we discovered that the light-stimulated growth was stronger in seawater with the single carbon compound alanine compared to a mixture of complex organic matter. Thus, differences between bacteria in PR gene expression regulation in response to light, nutrients or organic matter quality critically determine the ecological role of PR phototrophy in the sea.

    Current observations that membrane transporters (including PR) are highly expressed in seawater inspired a comparative analysis of transporter distributions in marine bacteria. Totally, 192 transporter families were found in 290 genome-sequenced strains. Consistent differences, but also similarities, in the number of transporters were found between major bacterial groups. Interestingly, sodium transporters were found to be more abundant in PR-containing SAR11. These findings suggest that bacteria have inherently distinctive potentials to adapt to resource variations in the sea.

    To examine links between transcriptional responses and growth of bacteria under controlled environmental settings, a mesocosm phytoplankton bloom experiment was performed. Transcriptional analysis of the microbial community (i.e. metatranscriptomics) revealed 2800 categories of functional genes (SEED functions), of which around 10% were overrepresented in either the bloom mesocosms or the controls. Importantly, these functions indicated potential metabolic mechanisms (e.g. TonB mediated nutrient transport) by which bacteria took advantage of the bloom conditions.

    This thesis combines analyses of model organisms with community analysis and highlights the possibilities to identify important mechanisms that underlie the ecological success of different bacteria in the marine environment. 

  • 2.
    Akram, Neelam
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Palovaara, Joakim
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Forsberg, Jeremy
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lindh, Markus V.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Milton, Debra L.
    Luo, Haiwei
    Gonzalez, Jose M.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Regulation of proteorhodopsin gene expression by nutrient limitation in the marine bacterium Vibrio sp AND42013In: Environmental Microbiology, ISSN 1462-2912, E-ISSN 1462-2920, Vol. 15, no 5, p. 1400-1415Article in journal (Refereed)
    Abstract [en]

    Proteorhodopsin (PR), a ubiquitous membrane photoprotein in marine environments, acts as a light-driven proton pump and can provide energy for bacterial cellular metabolism. However, knowledge of factors that regulate PR gene expression in different bacteria remains strongly limited. Here, experiments with Vibrio sp. AND4 showed that PR phototrophy promoted survival only in cells from stationary phase and not in actively growing cells. PR gene expression was tightly regulated, with very low values in exponential phase, a pronounced peak at the exponential/stationary phase intersection, and a marked decline in stationary phase. Thus, PR gene expression at the entry into stationary phase preceded, and could therefore largely explain, the stationary phase light-induced survival response in AND4. Further experiments revealed nutrient limitation, not light exposure, regulated this differential PR expression. Screening of available marine vibrios showed that the PR gene, and thus the potential for PR phototrophy, is found in at least three different clusters in the genus Vibrio. In an ecological context, our findings suggest that some PR-containing bacteria adapted to the exploitation of nutrient-rich micro-environments rely on a phase of relatively slowly declining resources to mount a cellular response preparing them for adverse conditions dispersed in the water column.

  • 3.
    Bunse, Carina
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Lundin, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Karlsson, Christofer M. G.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Akram, Neelam
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Vila-Costa, Maria
    Centre d’Estudis Avançats de Blanes-CSIC, Spain.
    Palovaara, Joakim
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Svensson, Lovisa
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Holmfeldt, Karin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    González, José M.
    University of La Laguna, Spain.
    Calvo, Eva
    Institut de Ciències del Mar—CSIC, Spain.
    Pelejero, Carles
    Institut de Ciències del Mar—CSIC, Spain.
    Marrasé, Cèlia
    Institut de Ciències del Mar—CSIC, Spain.
    Dopson, Mark
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Gasol, Josep
    Institut de Ciències del Mar—CSIC, Spain.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Response of marine bacterioplankton pH homeostasis gene expression to elevated CO22016In: Nature Climate Change, ISSN 1758-678X, E-ISSN 1758-6798, Vol. 6, no 5, p. 483-487Article in journal (Refereed)
    Abstract [en]

    Human-induced ocean acidification impacts marine life. Marine bacteria are major drivers of biogeochemical nutrient cycles and energy fluxes1; hence, understanding their performance under projected climate change scenarios is crucial for assessing ecosystem functioning. Whereas genetic and physiological responses of phytoplankton to ocean acidification are being disentangled2, 3, 4, corresponding functional responses of bacterioplankton to pH reduction from elevated CO2 are essentially unknown. Here we show, from metatranscriptome analyses of a phytoplankton bloom mesocosm experiment, that marine bacteria responded to lowered pH by enhancing the expression of genes encoding proton pumps, such as respiration complexes, proteorhodopsin and membrane transporters. Moreover, taxonomic transcript analysis showed that distinct bacterial groups expressed different pH homeostasis genes in response to elevated CO2. These responses were substantial for numerous pH homeostasis genes under low-chlorophyll conditions (chlorophyll a <2.5 μg l−1); however, the changes in gene expression under high-chlorophyll conditions (chlorophyll a >20 μg l−1) were low. Given that proton expulsion through pH homeostasis mechanisms is energetically costly, these findings suggest that bacterioplankton adaptation to ocean acidification could have long-term effects on the economy of ocean ecosystems.

  • 4.
    Gómez-Consarnau, Laura
    et al.
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Akram, Neelam
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Lindell, Kristoffer
    Pedersen, Anders
    Neutze, Richard
    Milton, Debra L.
    González, José M.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Science and Engineering, School of Natural Sciences.
    Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation2010In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 8, no 4, p. 1-10Article in journal (Refereed)
    Abstract [en]

    Proteorhodopsins are globally abundant photoproteins found in bacteria in the photic zone of the ocean. Although their function as proton pumps with energy-yielding potential has been demonstrated, the ecological role of proteorhodopsins remains largely unexplored. Here, we report the presence and function of proteorhodopsin in a member of the widespread genus Vibrio, uncovered through whole-genome analysis. Phylogenetic analysis suggests that the Vibrio strain AND4 obtained proteorhodopsin through lateral gene transfer, which could have modified the ecology of this marine bacterium. We demonstrate an increased long-term survival of AND4 when starved in seawater exposed to light rather than held in darkness. Furthermore, mutational analysis provides the first direct evidence, to our knowledge, linking the proteorhodopsin gene and its biological function in marine bacteria. Thus, proteorhodopsin phototrophy confers a fitness advantage to marine bacteria, representing a novel mechanism for bacterioplankton to endure frequent periods of resource deprivation at the ocean’s surface.

  • 5.
    Palovaara, Joakim
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Akram, Neelam
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Baltar, Federico
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Bunse, Carina
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Forsberg, Jeremy
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Pedrós-Alió, Carlos
    CSIC, Inst Ciencies Mar, Spain.
    González, José M.
    Univ La Laguna, Spain.
    Pinhassi, Jarone
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria2014In: 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)
    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.

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