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Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacterium Rheinheimera sp. BAL341
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. © 2019 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. ; Funding text #1 Received 8 April, 2019; revised 15 May, 2019; accepted 15 May, 2019. *For correspondence. E-mail jarone.pinhassi@lnu.se; Tel. +46725949448 Microbial Biotechnology (2019) 12(5), 892–906 doi:10.1111/1751-7915.13441 Funding Information. This research was supported by the BONUS BLUEPRINT project, which has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), and the Swedish research council FORMAS. Funding was also provided through the Swedish governmental strong research programme EcoChange (FORMAS). Work by ECG and MVC was supported by a Fundación BBVA award to MVC (14_CMA_020) and by the Spanish MEIC through the project ISOMICS (CTM2015-65691-R). Funding text #2 We thank Josef Lautin for excellent technical assistance in the laboratory and Prof. Jordi Dachs for advice on organic pollutants. The authors would like to acknowledge the support from Science for Life Laboratory, the National Genomics Infrastructure, NGI, and Uppmax for providing assistance in massive parallel sequencing and computational infrastructure. The computations were performed on resources provided by SNIC through Uppsala Multidisciplinary Center for Advanced Computational Funding text #3 Science (UPPMAX) under project b2011200. The research was supported by the BONUS BLUEPRINT project, which has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), and the Swedish research council FORMAS. Funding was also provided through the Swedish governmental strong research programme EcoChange (FORMAS). Work by ECG and MVC was supported by a Fundación BBVA award to MVC (14_CMA_020) and by the Spanish MEIC through the project ISOMICS (CTM2015-65691-R). ; Peer reviewed
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Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters
Thousands of semi-volatile hydrophobic organic pollutants (OPs) reach open oceans through atmospheric deposition, causing a chronic and ubiquitous pollution by anthropogenic dissolved organic carbon (ADOC). Hydrophobic ADOC accumulates in cellular lipids, inducing harmful effects on marine biota, and can be partially prone to microbial degradation. Unfortunately, their possible effects on microorganisms, key drivers of global biogeochemical cycles, remain unknown. We challenged coastal microbial communities from Ny-Ålesund (Arctic) and Livingston Island (Antarctica) with ADOC concentrations within the range of oceanic concentrations in 24 h. ADOC addition elicited clear transcriptional responses in multiple microbial heterotrophic metabolisms in ubiquitous groups such as Flavobacteriia, Gammaproteobacteria and SAR11. Importantly, a suite of cellular adaptations and detoxifying mechanisms, including remodelling of membrane lipids and transporters, was detected. ADOC exposure also changed the composition of microbial communities, through stimulation of rare biosphere taxa. Many of these taxa belong to recognized OPs degraders. This work shows that ADOC at environmentally relevant concentrations substantially influences marine microbial communities. Given that emissions of organic pollutants are growing during the Anthropocene, the results shown here suggest an increasing influence of ADOC on the structure of microbial communities and the biogeochemical cycles regulated by marine microbes. © 2019 Society for Applied Microbiology and John Wiley & Sons Ltd. ; This work was supported by BBVA Foundation for Researchers and Cultural Creative Workers award to MVC (14_CMA_020) and by the Spanish Ministerio de Economía y Competitividad (Ministry of Economy and Competitiveness, MEIC) through projects ISOMICS (CTM2015‐65691‐R), REMARCA (CTM2012‐34673) and SENTINEL (CTM2015‐70535‐P). ECG was supported by Agència de Gestió d'Ajuts Universtaris i Recerca, Generalitat de Catalunya (FI AGAUR) Scholarship, Generalitat de Catalunya Fellowship Program (Catalan Government, Generalitat de Catalunya). We thank MC. Fernández‐Pinos, M. Pizarro and G. Caballero for assistance with experimental settings, I. Forn, Dr. R. Massana and Dr. JM Gasol for support with CARD‐FISH and flow cytometry counts. Dr. C. Galbán‐Malagón (U. Andres‐Bello) for providing POP concentrations in polar seawater. The research group of Global Change and Genomic Biogeochemistry is supported by the Catalan Government (2017SGR800). ; Peer reviewed
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Microbial consumption of organophosphate esters in seawater under phosphorus limited conditions
The anthropogenic perturbation of the phosphorus (P) marine biogeochemical cycle due to synthetic organophosphorus compounds remains unexplored. The objective of this work was to investigate the microbial degradation of organophosphate triesters (OPEs), widely used as plasticizers and flame retardants, in seawater and their effects on the physiology and composition of microbial communities. Experiments were performed in July 2014 using surface seawater from the Blanes Bay Microbial Observatory (NW Mediterranean) to which OPEs were added at environmentally relevant concentrations. The concentrations of OPEs in the dissolved-phase generally decreased after 24 hours of incubation at in situ conditions. The fitted first order reaction constants were significantly different than zero for the trihaloalkyl phosphate, tris(2-chloroethyl) phosphate and trialyl phosphate tricresyl phosphate. In general, OPEs triggered an increase of the percentage of actively respiring bacteria, total bacterial activity, and the number of low-nucleic acid bacteria, and a decrease in the percentage of membrane-compromised bacteria. Members of some bacterial groups, in particular Flavobacteria, increased their specific activity, indicating that seawater contains bacteria with the potential to degrade OPEs. In aged seawater that was presumably depleted of labile dissolved organic carbon and inorganic P, alkaline phosphatase activities significantly decreased when OPEs were added, indicating a relief on P stress, consistent with the role of OPEs as potential P sources. © 2019, The Author(s). ; This work was supported by Fundación BBVA award to MVC and by the Spanish MEIC through projects ISOMICS (CTM2015-65691-R) and REMEI (CTM2015-70340-R). MS was supported by grant EcoRARE (CTM2014-60467-JIN), funded by the Spanish Government and the European Regional Development Fund (ERDF) and a Viera y Clavijo contract funded by the ACIISI and the ULPGC. The research group of Global Change and Genomic Biogeochemistry is supported by the Catalan Goverment (2017SGR800). We thank J Castro-Jimenez for support on the OPE analyses. MVC is indebted to J Pinhassi for support. ; Peer reviewed
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Bacterial responses to background organic pollutants in the northeast subarctic Pacific Ocean
Thousands of man-made synthetic chemicals are released to oceans and compose the anthropogenic dissolved organic carbon (ADOC). Little is known about the effects of this chronic pollution on marine microbiome activities. In this study, we measured the pollution level at three sites in the Northeast Subarctic Pacific Ocean (NESAP) and investigated how mixtures of three model families of ADOC at different environmentally relevant concentrations affected naturally occurring marine bacterioplankton communities' structure and metabolic functioning. The offshore northernmost site (North) had the lowest concentrations of hydrocarbons, as well as organophosphate ester plasticizers, contrasting with the two other continental shelf sites, the southern coastal site (South) being the most contaminated. At North, ADOC stimulated bacterial growth and promoted an increase in the contribution of some Gammaproteobacteria groups (e.g. Alteromonadales) to the 16 rRNA pool. These groups are described as fast responders after oil spills. In contrast, minor changes in South microbiome activities were observed. Gene expression profiles at Central showed the coexistence of ADOC degradation and stress-response strategies to cope with ADOC toxicities. These results show that marine microbial communities at three distinct domains in NESAP are influenced by background concentrations of ADOC, expanding previous assessments for polar and temperate waters. ; This publication is dedicated to the memory of our missed friend, mentor and colleague, Prof. Ronald P. Kiene. The authors thank the Capitan and crew of the R/V Oceanus. This work was funded by the Spanish MEIC through projects ISOMICS (CTM2015-65691-R) and SENTINEL (CTM2015-70535-P). The authors sincerely thank J.M. Gasol for support with flow cytometry counts and I. Forn for microscopy counts. The research group of Global Change and Genomic Biogeochemistry is supported by the Catalan Government (2017SGR800). IDAEA-CSIC is a Centre of Excellence Severo Ochoa (Spanish Ministry of Science and Innovation, Project CEX2018-000794-S). ; Peer reviewed
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