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Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacterium Rheinheimera sp. BAL341
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)
CSIC, Spain.ORCID iD: 0000-0001-9821-9227
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)ORCID iD: 0000-0002-8779-6464
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Ctr Ecol & Evolut Microbial Model Syst EEMiS)
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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. Vol. 12, no 5, p. 892-906
National Category
Microbiology
Research subject
Ecology, Microbiology
Identifiers
URN: urn:nbn:se:lnu:diva-86985DOI: 10.1111/1751-7915.13441ISI: 000474143400001PubMedID: 31270938Scopus ID: 2-s2.0-85068617751OAI: oai:DiVA.org:lnu-86985DiVA, id: diva2:1339057
Available from: 2019-07-25 Created: 2019-07-25 Last updated: 2019-11-25Bibliographically approved
In thesis
1. Exploring gene expression responses of marine bacteria to environmental factors
Open this publication in new window or tab >>Exploring gene expression responses of marine bacteria to environmental factors
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
Baltic Sea, dissolved organic matter, model bacteria, ocean acidification, organic pollutants, river loadings, transcriptomics
National Category
Ecology
Research subject
Ecology, Microbiology
Identifiers
urn:nbn:se:lnu:diva-90261 (URN)978-91-89081-19-2 (ISBN)978-91-89081-20-8 (ISBN)
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

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Karlsson, Christofer M. G.Lundin, DanielKarlsson, CamillaPinhassi, Jarone

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Karlsson, Christofer M. G.Cerro-Galvez, ElenaLundin, DanielKarlsson, CamillaVila-Costa, MariaPinhassi, Jarone
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