Biodegradation as an important sink of aromatic hydrocarbons in the oceans

González-Gaya, Belén; Martinez-Varela, Alícia; Vila‐Costa, Maria; Casal, Paulo; Cerro‐Gálvez, Elena; Berrojalbiz, Naiara; Lundin, Daniel; Vidal, Montserrat; Mompeán, Carmen; Bode, Antonio; Jiménez, Begoña; Dachs, Jordi

doi:10.1038/s41561-018-0285-3

Cited by 130 publications

(128 citation statements)

References 56 publications

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“…Still, field experiments performed in tropical seawaters have been able to detect a decrease in concentrations for n-alkanes after 24 h of incubation (Fernández-Pinos et al, 2017). Nevertheless, it is probable that many of the semi-labile dissolved ADOC components, such as individual n-alkanes, PAHs and HCHs, were being degraded after 24 h of incubation, since microbial degradation of these chemicals is known to occur in the marine environment (Galbán-Malagón et al, 2013a;González-Gaya et al, 2019). We next turned to molecular and genomic approaches to analyse the effects and potential use of ADOC.…”

Section: Dose-response Experiment: Exploratory Effects Of Fractions Omentioning

confidence: 99%

“…These correlations showed, for example, that transcripts coding for enzymes known to be involved in PAH degradation were correlated with concentrations of 2-4 ring PAHs. The degradation routes of aromatic hydrocarbons are among the best described (Mallick et al, 2011;González-Gaya et al, 2019). Aromatic hydrocarbons are one of the most abundant families of compounds in ADOC, and even though a significant correlation does not demonstrate a cause-effect relationship, the higher expression of the Pfam ring hydroxyl A and B in ADOC treatments may be coupled to PAH degradation.…”

Section: Changes In Bacterioplankton Community Compositionmentioning

confidence: 99%

“…Therefore, both n-alkanes and OPEs were not enriched necessarily in the incubations, but showed a variability in their dissolved concentrations due to either microbial mediated processes (degradation, sorption) or manipulation artefacts (sorption to bottle walls…). Analyses were performed following the procedures described elsewhere (Berrojalbiz et al, 2009;Fernández-Pinos et al, 2017;González-Gaya et al, 2019;Vila-Costa et al, 2019). See Supporting Information for details.…”

Section: Concentrations Of Selected Adoc Compounds In the Experimentsmentioning

confidence: 99%

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Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

Cerro‐Gálvez

Casal

Lundin

et al. 2019

Environmental Microbiology

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Summary 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.

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Section: Dose-response Experiment: Exploratory Effects Of Fractions Omentioning

confidence: 99%

Section: Changes In Bacterioplankton Community Compositionmentioning

confidence: 99%

Section: Concentrations Of Selected Adoc Compounds In the Experimentsmentioning

confidence: 99%

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Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

Cerro‐Gálvez

Casal

Lundin

et al. 2019

Environmental Microbiology

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“…Aromatic ring-hydroxylating dioxygenases (RHDO, alpha and beta subunits) are used as robust markers of PAH biodegradation (González-Gaya, Martínez-Varela et al 2019). Primers designed to amplify various RHDOs from Gram-negative and Gram-positive bacteria have been successfully used to differentiate oil-contaminated seawater of the Yellow sea from uncontaminated (Wang, Zhang et al 2014).…”

Section: Upregulated Functionsmentioning

confidence: 99%

Discovery of functional gene markers of bacteria for monitoring hydrocarbon pollution in the marine environment - a metatranscriptomics approach

Knapik

Bagi

Królicka

et al. 2019

Preprint

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The use of natural marine bacteria as "oil sensors" for the detection of pollution events can be suggested as a novel way of monitoring oil occurrence at sea. Nucleic acid-based devices generically called genosensors are emerging as potentially promising tools for in situ detection of specific microbial marker genes suited for that purpose. Functional marker genes are particularly interesting as targets for oil-related genosensing but their identification remains a challenge. Here, seawater samples, collected in tanks with oil addition mimicking a realistic oil spill scenario, were filtered and archived by the Environmental Sample Processor (ESP), a fully robotized genosensor, and the samples were then used for post-retrieval metatranscriptomic analysis. After extraction, RNA from ESP-archived samples at start, day 4 and day 7 of the experiment was used for sequencing. Metatranscriptomics revealed that several KEGG pathways were significantly enriched in samples exposed to oil. However, these pathways were highly expressed also in the non-oil-exposed water samples, most likely as a result of the release of natural organic matter from decaying phytoplankton. Temporary peaks of aliphatic alcohol and aldehyde dehydrogenases and monoaromatic ringdegrading enzymes (e.g. ben, box, and dmp clusters) were observed on day 4 in both control and oil tanks. Few alkane 1-monooxygenase genes were upregulated on oil, mostly transcribed by families Porticoccaceae and Rhodobacteraceae, together with aromatic ring-hydroxylating dioxygenases, mostly transcribed by Rhodobacteraceae. Few transcripts from obligate hydrocarbonoclastic genera of Alcanivorax, Oleispira and Cycloclasticus, were significantly enriched in the oil-treated tank in comparison to control, and these were mostly transporters and genes involved in nitrogen and phosphorous acquisition. This study highlights the importance of seasonality, i.e., phytoplankton occurrence and senescence leading to organic compound release which can be used preferentially by bacteria over oil compounds, delaying the latter process. As a result, such seasonal effect can reduce the sensitivity of genosensing tools employing bacterial functional genes to sense oil. A better understanding of the use of natural organic matter by bacteria involved in oil-biodegradation is needed to develop an array of functional markers enabling the rapid and specific in situ detection of anthropogenic pollution.

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“…Bacterioplankton are a key component of marine ecosystems, where they are responsible for the transformation of organic and inorganic nutrients in the water column (Azam, ; Falkowski et al ., ). The bacteria play a central role in the biogeochemical carbon cycle since they are the main consumers of dissolved organic carbon (DOC), one of the largest reservoirs of carbon in seawater (Azam et al ., ), and they are also expected to play a major role in the cycling of OPs (Del Vento and Dachs, ; González‐Gaya et al ., ). Hydrocarbons in the marine environment can stimulate the growth rates of bacteria and also select for specific bacterial groups (for example members of the genera Cycloclasticus , Marinobacter , Oceanospirillum ) (Zobell, ; Leahy and Colwell, ; Teira et al ., ; Seo et al ., ; Rivers et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacteriumRheinheimerasp.BAL341

Karlsson

Cerro‐Gálvez

Lundin

et al. 2019

Microbial Biotechnology

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Summary 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.

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Biodegradation as an important sink of aromatic hydrocarbons in the oceans

Cited by 130 publications

References 56 publications

Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

Discovery of functional gene markers of bacteria for monitoring hydrocarbon pollution in the marine environment - a metatranscriptomics approach

Direct effects of organic pollutants on the growth and gene expression of the Baltic Sea model bacteriumRheinheimerasp.BAL341

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