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.

Responses of Coastal Marine Microbiomes Exposed to Anthropogenic Dissolved Organic Carbon.

Coastal seawaters receive thousands of organic pollutants. However, we have little understanding of the response of microbiomes to this pool of anthropogenic dissolved organic carbon (ADOC). In this study, coastal microbial communities were challenged with ADOC at environmentally relevant concentrations. Experiments were performed at two Mediterranean sites with different impact by pollutants and nutrients: off the Barcelona harbor ("BCN"), and at the Blanes Bay ("BL"). ADOC additions stimulated prokaryotic leucine incorporation rates at both sites, indicating the use of ADOC as growth substrate. The percentage of "membrane-compromised" cells increased with increasing ADOC, indicating concurrent toxic effects of ADOC. Metagenomic analysis of the BCN community challenged with ADOC showed a significant growth of Methylophaga and other gammaproteobacterial taxa belonging to the rare biosphere. Gene expression profiles showed a taxon-dependent response, with significantly enrichments of transcripts from SAR11 and Glaciecola spp. in BCN and BL, respectively. Further, the relative abundance of transposon-related genes (in BCN) and transcripts (in BL) correlated with the number of differentially abundant genes (in BCN) and transcripts (in BLA), suggesting that microbial responses to pollution may be related to pre-exposure to pollutants, with transposons playing a role in adaptation to ADOC. Our results point to a taxon-specific response to low concentrations of ADOC that impact the functionality, structure and plasticity of the communities in coastal seawaters. This work contributes to address the influence of pollutants on microbiomes and their perturbation to ecosystem services and ocean health.

Legacy and novel flame retardants from indoor dust in Antarctica: Sources and human exposure.

The air humidity in Antarctica is very low and this peculiar weather parameter make the use of flame retardants in research facilities highly needed for safety reasons, as fires are a major risk. Legacy and novel flame retardants (nFRs) including polybrominated diphenyl ethers (PBDEs), hexabromocyclododecanes (HBCDs), 1,2-bis(2,4,6-tribromophenoxy) ethane (BTBPE), Dechlorane Plus (DP), and other nFRs were measured in indoor dust samples collected at research Stations in Antarctica: Gabriel de Castilla, Spain (GCS), Julio Escudero, Chile (JES), and onboard the RRS James Clark Ross, United Kingdom (RRS JCR). The GC-HRMS and LC-MS-MS analyses of dust samples revealed ∑7PBDEs of 41.5 ± 43.8 ng/g in rooms at GCS, 18.7 ± 11.6 ng/g at JES, and 27.2 ± 37.9 ng/g onboard the RRS JCR. PBDE pattern was different between the sites and most abundant congeners were BDE-183 (40%) at GCS, BDE-99 (50%) at JES, and BDE-153 (37%) onboard the RRS JCR. The ∑(4)HBCDs were 257 ± 407 ng/g, 14.9 ± 14.5 ng/g, and 761 ± 1043 ng/g in indoor dust collected in rooms at GCS, JES, and RRS JCR, respectively. The ∑9nFRs were 224 ± 178 ng/g at GCS, 14.1 ± 13.8 ng/g at JES, and 194 ± 392 ng/g on the RRS JCR. Syn- and anti-DP were detected in most of the samples and both isomers showed the highest concentrations at GCS: 163 ± 93.6 and 48.5 ± 61.1 ng/g, respectively. The laboratory and living room showed the highest concentration of HBCDs, DPs, BTBPE. The wide variations in FR levels in dust from the three research facilities and between differently used rooms reflect the different origin of furnishing, building materials and equipment. The potential health risk associated to a daily exposure via dust ingestion was assessed for selected FRs: BDEs 47, 99, and 153, α-, ß-, and γ-HBCD, BTBPE, syn- and anti-DP. Although the estimated exposures are below the available reference doses, caution is needed given the expected increasing use of novel chemicals without a comprehensive toxicological profile.

Anthropogenic dissolved organic carbon and marine microbiomes.

Thousands of synthetic chemicals and hydrocarbons are released to the marine environment composing the anthropogenic dissolved organic carbon (ADOC). Most ADOC is disproportionally hydrophobic, and consequently, its concentrations in the cell membranes are between a thousand and hundred million fold higher than those in the dissolved phase. Marine microorganisms respond to ADOC by multiple strategies ranging from ADOC degradation to detoxifying metabolisms. We argue that the increasing concentrations of ADOC in the oceans deriving from rivers, atmospheric deposition, and plastic leachates can have an effect on the health of the oceans and influence the major biogeochemical cycles, thus influencing the Earth system during the Anthropocene.

Microbial responses to perfluoroalkyl substances and perfluorooctanesulfonate (PFOS) desulfurization in the Antarctic marine environment.

Perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) acids are ubiquitous in the oceans, including remote regions, and are toxic to fish and mammals. The impact to the lowest trophic levels of the food web, however, remains unknown. We challenged natural bacterial communities inhabiting Antarctic coastal waters (Deception Island) with PFOS and PFOA concentrations ranging from 2 ng/L to 600 ng/L that selected for tolerant taxa. After 48 h, concentrations of PFOS decreased by more than 50% and sulfur metabolism-related transcripts were significantly enriched in the treatments suggesting desulfurization of PFOS. Conversely, no significant differences were found between initial and final PFOA concentrations. Gammaproteobacteria and Roseobacter, two abundant groups of marine bacteria, increased their relative activity after 24 h of incubation, whereas Flavobacteriia became the main contributor in the treatments after 6 days. Community activities (extracellular enzyme activity and absolute number of transcripts) were higher in the treatments than in the controls, while bacterial abundances were lower in the treatments, suggesting a selection of PFOS and PFOA tolerant community in the exposed treatments. Our results show a direct effect of PFOS and PFOA exposure on the composition and functionality of natural Antarctic marine microbial communities. While no evidence of defluorination of PFOS or PFOA was detected, probable desulfurization of PFOS depicts a direct link with the sulfur biogeochemistry of the ocean.

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.

Modulation of microbial growth and enzymatic activities in the marine environment due to exposure to organic contaminants of emerging concern and hydrocarbons.

Organic pollutants are continuously being introduced in seawater with uncharacterized impacts on the engines of the marine biogeochemical cycles, the microorganisms. The effects on marine microbial communities were assessed for perfluoroalkyl substances, organophosphate esters flame retardants and plasticizers, polycyclic aromatic hydrocarbons, and n-alkanes. Dose-response experiments were performed at three stations and at three depths in the NW Mediterranean with contrasted nutrient and pollutant concentrations. In these experiments, the microbial growth rates, the abundances of the main bacterial groups, measured by Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (CARD-FISH), and extracellular enzymatic activities, were quantified. Increasing concentrations of organic pollutants (OPs) promoted different responses in the communities that were compound, organism and nutrient availability (trophic status). The largest differences between OP treatments and controls in the growth rates of both heterotrophic and phototrophic microbial groups were observed in seawater from the deep chlorophyll maxima. Furthermore, there was a compound specific stimulation of different extracellular enzymatic activities after the exposure to OPs. Our results revealed that marine microbial communities reacted not only to hydrocarbons, known to be used as a carbon source, but also to low concentrations of organic pollutants of emerging concern in a complex manner, reflecting the variability of various environmental variables. Multiple linear regressions suggested that organic pollutants modulated the bacterial growth and extracellular enzymatic activities, but this modulation was of lower magnitude than the observed pronounced response of the microbial community to nutrient availability.

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.

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.