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Exploring gene expression responses of marine bacteria to environmental factors
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Marine microbiology)ORCID iD: 0000-0001-6866-8881
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Bacterioplankton are abundant in marine ecosystems, where they as “masters of transformation” of dissolved organic matter (DOM) are important for energy fluxes and biogeochemical cycles. However, the performance of bacteria in a changing marine environment influenced by anthropogenic activities is poorly understood. In this thesis, I did experiments with model bacteria and natural assemblages of bacteria, using microbiology methods combined with modern molecular tools, to investigate responses of marine bacteria to changes in environmental conditions like ocean acidification, organic pollution and organic matter released by phytoplankton. Experiments with a model gammaproteobacterium demonstrated that bacteria in stationary phase showed little responses to organic pollutants, whereas pollutants caused decreased bacterial growth and had a broad physiological impact on actively growing bacteria (as deduced from gene expression analysis). In an experiment with two distantly related marine model bacteria, we identified several important bacterial mechanisms, such as uptake of macromolecules and phosphonates, by which bacteria respond when exposed to DOM produced by photosynthetic dinoflagellates. Using natural bacterial communities in a Baltic Sea mesocosm experiment with the addition of river water from a forested or an agriculture influenced catchment area, we showed important interactions between river water type and the development of phytoplankton blooms that caused different bacterial gene expression activities. In the fourth set of experiments, marine bacterial communities were subjected to elevated CO2, to mimic ocean acidification, under high and low nutrient conditions in a mesocosm study. We found increased bacterial gene expression activity focused on maintaining pH homeostasis, but only under low nutrient conditions, indicating that bacteria focus on cell maintenance instead of growth when challenged by lowered pH. Finally, in a computational analysis, we compared genomes from yet uncultivated prokaryotes by two different strategies: metagenome assembled and single amplified genomes. Importantly, the analysis showed that both methods selected abundant taxa and generated nearly identical sequences in overlapping regions. To conclude, this thesis presents discoveries that will help form a better understanding of marine bacterial responses to present and future anthropogenic disturbances of marine ecosystems.

Abstract [sv]

Marina bakterier är abundanta och återfinns i alla marina ekosystem, där de som nedbrytare av organiskt material spelar en avgörande roll i att reglera flödet av energi och näringsämnenas kretslopp. Dock saknar vi kunskap om hur bakterieplankton reagerar på miljöförändringar i haven. Därtill är de molekylära mekanismerna för omsättningen av löst organiskt material från olika källor ofullständigt kända. I denna avhandling har jag med hjälp av bakterieisolat och naturliga bakteriesamhällen undersökt hur marina bakterier svarar på miljöförändringar genom att kombinera metoder inom klassisk mikrobiologi och moderna molekylärbiologiska verktyg. Det övergripande syftet med denna avhandling var att få en bättre förståelse för hur bakterier svarar på havsförsurning, organiska föroreningar och löst organisk kol utsöndrat av växtplankton. Under ett experiment med ett bakterieisolat inom klassen Gammaproteobacteria, uppvisade bakterierna svagare respons för organiska föroreningar då de befann sig i stationär fas än i en aktiv tillväxtfas. Detta märktes både genom minskad tillväxt och fysiologiska ändringar uppmätta genom genuttryck i bakterien. Vidare experiment med två skilda modellbakterier kunde vi identifiera viktiga processer såsom upptag av makromolekyler och fosfonater, som svar på tillsats av löst organiskt material producerat av dinoflagellater. I ett annat experiment använde vi naturliga bakteriesamhällen i vatten från Östersjön i ett storskaligt experiment, där vatten från floder i avrinningsområden dominerade antingen av skog eller jordbruk tillsattes. I detta experiment kunde vi visa hur vattnets ursprung påverkade utvecklingen av algblomningarna som i sin tur orsakade olika aktivitet i bakteriernas genuttryck. Vidare så undersöktes hur marina bakteriesamhällen påverkas av förhöjda CO2-halter under låg och hög näringstillgång. Det visade sig att bakterierna ökade sin aktivitet för att bibehålla pH-homeostasen, men bara under låg koncentration av näringsämnen. Detta innebar att bakterierna behövde ställa om sin ämnesomsättning från tillväxt till att lägga energi på att hantera syran i oligotrofa miljöer. Slutligen genomfördes dataanalyser där två metoder för att studera arvsmassan i bakterier tagna direkt från haven jämfördes. Vår studie visade att de två metoderna i viss mån kompletterade varandra men framför allt kunde vi bekräfta att ingen av de två uppvisade några systematiska fel. Sammanfattningsvis presenterar denna avhandling upptäcker som ger oss en bättre förståelse för hur marina bakterier i marina ekosystem svarar på nutida och framtida miljöförändringar orsakade av människor.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2019.
Series
Linnaeus University Dissertations ; 371/2019
Keywords [en]
Baltic Sea, dissolved organic matter, model bacteria, ocean acidification, organic pollutants, river loadings, transcriptomics
National Category
Ecology
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-90261ISBN: 978-91-89081-19-2 (print)ISBN: 978-91-89081-20-8 (electronic)OAI: oai:DiVA.org:lnu-90261DiVA, id: diva2:1372912
Public defence
2019-12-18, Fregatten Ma117 campus Kalmar, Kalmar, 09:30 (English)
Opponent
Supervisors
Available from: 2019-11-25 Created: 2019-11-25 Last updated: 2019-12-03Bibliographically approved
List of papers
1. Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes
Open this publication in new window or tab >>Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes
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2018 (English)In: Microbiome, ISSN 0026-2633, E-ISSN 2049-2618, Vol. 6, article id 173Article in journal (Refereed) Published
Abstract [en]

Background: Prokaryotes dominate the biosphere and regulate biogeochemical processes essential to all life. Yet, our knowledge about their biology is for the most part limited to the minority that has been successfully cultured. Molecular techniques now allow for obtaining genome sequences of uncultivated prokaryotic taxa, facilitating in-depth analyses that may ultimately improve our understanding of these key organisms. Results: We compared results from two culture-independent strategies for recovering bacterial genomes: single-amplified genomes and metagenome-assembled genomes. Single-amplified genomes were obtained from samples collected at an offshore station in the Baltic Sea Proper and compared to previously obtained metagenome-assembled genomes from a time series at the same station. Among 16 single-amplified genomes analyzed, seven were found to match metagenome-assembled genomes, affiliated with a diverse set of taxa. Notably, genome pairs between the two approaches were nearly identical (average 99.51% sequence identity; range 98.77-99.84%) across overlapping regions (30-80% of each genome). Within matching pairs, the single-amplified genomes were consistently smaller and less complete, whereas the genetic functional profiles were maintained. For the metagenome-assembled genomes, only on average 3.6% of the bases were estimated to be missing from the genomes due to wrongly binned contigs. Conclusions: The strong agreement between the single-amplified and metagenome-assembled genomes emphasizes that both methods generate accurate genome information from uncultivated bacteria. Importantly, this implies that the research questions and the available resources are allowed to determine the selection of genomics approach for microbiome studies.

Place, publisher, year, edition, pages
BioMed Central, 2018
Keywords
Single-amplified genomes, Metagenome-assembled genomes, Metagenomics, Binning, Single-cell genomics
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-78465 (URN)10.1186/s40168-018-0550-0 (DOI)000446307400001 ()30266101 (PubMedID)2-s2.0-85054254141 (Scopus ID)
Available from: 2018-10-24 Created: 2018-10-24 Last updated: 2019-11-25Bibliographically approved
2. Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2
Open this publication in new window or tab >>Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2
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2016 (English)In: Nature Climate Change, ISSN 1758-678X, E-ISSN 1758-6798, Vol. 6, no 5, p. 483-487Article in journal (Refereed) Published
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.

National Category
Microbiology Ecology Climate Research
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-49969 (URN)10.1038/nclimate2914 (DOI)000375125200015 ()2-s2.0-84964949342 (Scopus ID)
Projects
EcoChange
Available from: 2016-02-29 Created: 2016-02-29 Last updated: 2019-11-25Bibliographically approved
3. Metatranscriptomic analysis uncovers divergent responses of Baltic Sea bacteria to forest and agriculture river loadings
Open this publication in new window or tab >>Metatranscriptomic analysis uncovers divergent responses of Baltic Sea bacteria to forest and agriculture river loadings
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Climate change is predicted to induce substantial changes in precipitation patterns across the globe. In Northern Europe, precipitation is expected to increase more than the global average (particularly in northern Scandinavia), causing increased river runoff. The Baltic Sea is one of the largest brackish environments on earth with a catchment area that spans 14 countries, encompassing primarily forested areas and agricultural landscapes. Despite the acknowledged role of marine bacteria in nutrient cycling, there is a lack of knowledge in their metabolic responses to inorganic and organic nutrient loading from riverine runoff. We investigated the bacterial growth and gene expression responses in a mesocosm experiment in which river water from boreal forest- (enriched in humic substances) or agriculture- influenced catchment areas were added to Baltic Sea Proper water. The riverine nutrient input triggered extensive phytoplankton blooms and bacterial growth, most notably in the agriculture river treatment. Interestingly, bacterial gene expression analysis (metatranscriptomics) showed similar responses to agriculture and humic river inputs at the start of the experiment (before the phytoplankton bloom), but expression patterns diverged significantly upon bloom senescence.Notably, transcripts associated with phosphate metabolism were significantly enriched , whereas transcripts related to nitrogen metabolism were significantly lower in the agriculture river treatment compared to the boreal forest river treatment. The opposite pattern was observed in the boreal forest river water treatment. Overall, our results showed that interactions between river nutrient loading and phytoplankton organic matter are important in regulating bacterial activities and responses at the molecular level. This suggests that bacterial transformations of organic matter and nutrient cycling in coastal waters and estuarine environments are sensitive to changes in precipitation patterns in a catchment area-dependent manner.

Keywords
Marine bacteria, nutrient loading, dissolved organic carbon, dissolved organic nitrogen, phytoplankton bloom, humic substances
National Category
Biological Sciences
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-90254 (URN)
Available from: 2019-11-25 Created: 2019-11-25 Last updated: 2019-11-29Bibliographically approved
4. Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacterium Rheinheimera sp. BAL341
Open this publication in new window or tab >>Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacterium Rheinheimera sp. BAL341
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2019 (English)In: Microbial Biotechnology, ISSN 1751-7907, E-ISSN 1751-7915, Vol. 12, no 5, p. 892-906Article in journal (Refereed) Published
Abstract [en]

Organic pollutants (OPs) are critically toxic, bioaccumulative and globally widespread. Moreover, several OPs negatively influence aquatic wildlife. Although bacteria are major drivers of the ocean carbon cycle and the turnover of vital elements, there is limited knowledge of OP effects on heterotrophic bacterioplankton. We therefore investigated growth and gene expression responses of the Baltic Sea model bacterium Rheinheimera sp. BAL341 to environmentally relevant concentrations of distinct classes of OPs in 2-h incubation experiments. During exponential growth, exposure to a mix of polycyclic aromatic hydrocarbons, alkanes and organophosphate esters (denoted MIX) resulted in a significant decrease (between 9% and 18%) in bacterial abundance and production compared with controls. In contrast, combined exposure to perfluorooctanesulfonic acids and perfluorooctanoic acids (denoted PFAS) had no significant effect on growth. Nevertheless, MIX and PFAS exposures both induced significant shifts in gene expression profiles compared with controls in exponential growth. This involved several functional metabolism categories (e.g. stress response and fatty acids metabolism), some of which were pollutant-specific (e.g. phosphate acquisition and alkane-1 monooxygenase genes). In stationary phase, only two genes in the MIX treatment were significantly differentially expressed. The substantial direct influence of OPs on metabolism during bacterial growth suggests that widespread OPs could severely alter biogeochemical processes governed by bacterioplankton.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-86985 (URN)10.1111/1751-7915.13441 (DOI)000474143400001 ()31270938 (PubMedID)2-s2.0-85068617751 (Scopus ID)
Available from: 2019-07-25 Created: 2019-07-25 Last updated: 2019-11-25Bibliographically approved
5. Different gene expression responses in two Baltic Sea heterotrophic model bacteria to dinoflagellate dissolved organic matter
Open this publication in new window or tab >>Different gene expression responses in two Baltic Sea heterotrophic model bacteria to dinoflagellate dissolved organic matter
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Phytoplankton release massive amounts of dissolved organic matter (DOM) into the water column during recurring blooms in coastal waters and inland seas. The released DOM includes dissolved organic carbon, nitrogen and phosphorus, in a complex mixture of both known and unknown compounds, and is a rich nutrient source for heterotrophic bacteria. The metabolic activity of heterotrophic bacteria during and after phytoplankton blooms can hence be expected to reflect the characteristics of the released DOM. With this in mind, we wanted to investigate if bacterioplankton could be used as “living sensors” of phytoplankton DOM quantity and quality, and to trace the flow of nutrients in the ecosystem. We used transcriptional activity from Baltic Sea bacterial isolates (Polaribacter sp. BAL334 (Flavobacteriia) and Brevundimonas sp. BAL450 (Alphaproteobacteria)) exposed to DOM derived from the dinoflagellate Prorocentrum minimum in exponential and stationary growth phases respectively. We observed strong responses both in terms of physiology – bacterial abundance – and the expressed metabolic pathways – e.g. Membrane Transport, Fatty Acids, Lipids and Isoprenoids – of the populations in samples exposed to dinoflagellate DOM compared with controls. Particularly striking was the increased expression of Ton and Tol transport systems, commonly associated with uptake of complex molecules, in both isolates. Equally important were the differences in metabolic responses between the two isolates, caused by differences in gene repertoire between them, emphasizing the importance of separating the responses of different taxa in analyses of community sequence data. Differences in response to DOM sourced from exponentially and stationary growing dinoflagellates were less pronounced, although not absent, than differences between the bacterial isolates. This suggests that shifts in metabolism during the different phases of a phytoplankton bloom might be detectable in individual bacterial populations. To conclude, our work opened a door to the future use of bacterioplankton as living sensors of environmental status, particularly with respect to phytoplankton blooms.

Keywords
Alphaproteobacteria, Brevundimonas sp., Flavobacteria, mRNA, phytoplankton exudation, Polaribacter sp., Prorocentrum minimum
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-90255 (URN)
Available from: 2019-11-25 Created: 2019-11-25 Last updated: 2019-11-29Bibliographically approved

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