Response of oligotrophic coastal microbial populations in the SE Mediterranean Sea to crude oil pollution; lessons from mesocosm studies

Shai, Yael; Rubin‐Blum, Maxim; Angel, Dror L.; Sisma-Ventura, Guy; Zurel, Dror; Astrahan, Peleg; Rahav, Eyal

doi:10.1016/j.ecss.2020.107102

Cited by 18 publications

(9 citation statements)

References 65 publications

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“…The higher number of transcriptionally responding MAGs in the Atlantic than in the Pacific experiments can be related to the more oligotrophic status of Atlantic waters, where ADOC addition represented a more relevant pulse of carbon than in the Pacific. This is consistent with the higher sensitivity of oligotrophic systems to external anthropogenic inputs (Shai et al, 2021). Our results indicate that this is also true at ADOC concentrations relevant for the open ocean, as previously reported for coastal Mediterranean waters (Cerro-Gálvez et al, 2021).…”

Section: Responses Of Mags In Adoc Exposed Communitiessupporting

confidence: 92%

Responses to organic pollutants in the tropical Pacific and subtropical Atlantic Oceans by pelagic marine bacteria

Vila‐Costa

Lundin

Fernández-Pinos

et al. 2023

Front. Environ. Sci.

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Background and chronic pollution by organic pollutants (OPs) is a widespread threat in the oceans with still uncharacterized effects on marine ecosystems and the modulation of major biogeochemical cycles. The ecological impact and toxicity of this anthropogenic dissolved organic carbon (ADOC) is not related to the presence of a single compound but to the co-occurrence of a myriad of synthetic chemicals with largely unknown effects on heterotrophic microbial communities. We have analyzed the metabolic capacity of metagenome-assembled genomes (MAGs) of natural oceanic communities from the north Pacific (Costa Rica dome) and Atlantic oceans challenged with environmentally relevant levels of ADOC. In the Atlantic, ADOC-exposed MAGs responded transcriptionally more strongly compared to controls than in the Pacific, possibly mirroring the higher relevance of ADOC compounds as carbon source in oligotrophic environments. The largest proportions of transcripts originated from MAGs belonging in the families Rhodobacteraceae and Flavobacteriaceae, known to play a role on consumption of several OPs. In the Atlantic, archaeal Poseidoniales showed the highest transcription levels after 2 h of ADOC exposure, although no increase of relative abundances in the DNA pool was recorded after 24 h, whereas Methylophaga showed the opposite pattern. Both taxa are suggested to be actively involved in the consumption of biogenic alkanes produced by cyanobacteria. We observed similar gene expression profiles of alkane degradation and methylotrophy signature genes. These findings, plus the chemical degradation of alkanes measured in the experiments, provides experimental evidence of the consumption of anthropogenic hydrocarbons and synthetic chemicals at the low concentrations found in the ocean, and modulation of microbiomes by ADOC.

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Section: Responses Of Mags In Adoc Exposed Communitiessupporting

confidence: 92%

Responses to organic pollutants in the tropical Pacific and subtropical Atlantic Oceans by pelagic marine bacteria

Vila‐Costa

Lundin

Fernández-Pinos

et al. 2023

Front. Environ. Sci.

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“…Heins et al identified a bacterial strain related to clade BD1-7 in bloom samples and observed frequent occurrences of Spongiibacteraceae on particles [ 48 ]. Moreover, Spongiibacteraceae has been recognized as potential oil-degrading bacteria within microbial communities during oil spill experiments [ 49 ]. Further investigation of Spongiibacteraceae in relation to A. catenella could shed light on the mechanisms behind A. catenella blooms from an algal-bacterial mutualistic perspective.…”

Section: Discussionmentioning

confidence: 99%

Identification of bacteria in potential mutualism with toxic Alexandrium catenella in Chilean Patagonian fjords by in vitro and field monitoring

Yarimizu,

Mardones,

Paredes-Mella

et al. 2024

PLoS ONE

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The dinoflagellate Alexandrium catenella is a well-known paralytic shellfish toxin producer that forms harmful algal blooms, repeatedly causing damage to Chilean coastal waters. The causes and behavior of algal blooms are complex and vary across different regions. As bacterial interactions with algal species are increasingly recognized as a key factor driving algal blooms, the present study identifies several bacterial candidates potentially associated with Chilean Alexandrium catenella. This research narrowed down the selection of bacteria from the Chilean A. catenella culture using antibiotic treatment and 16S rRNA metabarcoding analysis. Subsequently, seawater from two Chilean coastal stations, Isla Julia and Isla San Pedro, was monitored for two years to detect Alexandrium species and the selected bacteria, utilizing 16S and 18S rRNA gene metabarcoding analyses. The results suggested a potential association between Alexandrium species and Spongiibacteraceae at both stations. The proposed candidate bacteria within the Spongiibacteraceae family, potentially engaging in mutualistic relationships with Alexandrium species, included the genus of BD1-7 clade, Spongiibbacter, and Zhongshania.

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“…The overall minor changes in heterotrophic microbial variables exposed to hydrocarbons may be explained in several not mutually exclusive ways: 1) Hydrocarbon degraders that were present before the amendments may become active at the expense of non-hydrocarbon degrading bacteria. Under these circumstances, bacterial abundance may not necessarily change, but selection of more tolerant microbes may occur, and bacterial activity is expected to increase; 2) Macronutrients such as N or P may limit bacterial growth post hydrocarbon additions (Shai et al, 2021) and 3) toxic effects of some PAH molecules (e.g., Naphthalene and\or benzo(a)pyrene, Supplementary Table S2) reduce bacterial growth variables (excluding hydrocarbon degraders). The decrease in NO 2 − + NO 3 − levels following crude oil or gas condensate additions relative to the controls in the first ~100 days post-addition (Figures 2A,B and Supplementary Table S1), was likely due to increased bacterial use through assimilation and denitrification, accompanied by elevated bacterial production rates (Figures 3C,D and Supplementary Table S1).…”

Section: Hydrocarbons Reach Nearshore Sediments and Alter Microbial A...mentioning

confidence: 99%

“…Gas-condensate is a mixture of light hydrocarbons formed by the condensation of hydrocarbon vapors from oil or gas deposits (Gieg et al, 1999;Faramawy et al, 2016) and is considered an acutely toxic petroleum hydrocarbon mixture that behaves differently to the heavier crude-oil in the marine environment (Øksenvåg et al, 2017). Hydrocarbon spills may limit gas exchange across the air-sea interface (Hasse and Liss, 1980), reduce phytoplankton abundance and primary productivity rates (Abbriano et al, 2011;Shai et al, 2021), alter the microbial abundance, diversity and function (Hazen et al, 2010;Brussaard et al, 2016) and kill many zooplankton species (Almeda et al, 2016). These spills often increase total heterotrophic bacterial abundances and activities, while reducing bacterial diversity (Lee and Levy, 1989;Joel et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…To date, most studies of MOSSFA and its effects on marine ecology focused on the Gulf of Mexico and Arctic regions (Gregson et al, 2021). Little is known regarding the effects of hydrocarbon pollution on benthic microbial populations in oligotrophic basins, such as the southeastern Mediterranean Sea, an enclosed and oligotrophic basin that may be highly sensitive to environmental perturbations (Shai et al, 2021). The southeastern Mediterranean Sea offshore Israel is highly susceptible to oil-based contaminants that may impact the sediment, especially in shallow littoral-coastal areas, due to the widespread extraction of natural gas deposits and transport of byproducts, such as gas-condensate (Shaffer, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Effects of crude oil and gas condensate spill on coastal benthic microbial populations

Kababu

Angel

Sisma-Ventura

et al. 2022

Front. Environ. Sci.

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Marine sediments are ecologically-important environments that act as a long-term depository for different contaminants from natural and anthropogenic sources. We investigated the response of crude-oil and gas-condensate spills on benthic microbial populations in the oligotrophic southeastern Mediterranean Sea using costume-design benthocosms. Additions of crude oil and gas condensate significantly changed the sediment’s chemical properties, with 2-fold elevated levels of total organic carbon (TOC) and up to ∼ 6-fold higher concentration of total polycyclic aromatic hydrocarbons (∑PAHs) relative to unamended sediments. Naphthalene and benzo(a)pyrene were the dominant species comprising the PAHs in both the crude-oil and gas-condensate treatments (29–43% and 26–35%, respectively). Porewater PO43+ drastically declined throughout the experiment, whereas NO2− + NO3− decreased ∼100 days post hydrocarbons addition and then increased in the remaining ∼100 days till the conclusion of the experiment. This temporal variability in NO2− + NO3− hints that hydrocarbon pollution may affect the interplay between benthic denitrification and N2 fixation, thus affecting nutrient limitation for benthic heterotrophic bacteria and phytoplankton. Moreover, our results show that crude oil and gas-condensate usually lead to a decline in benthic autotrophic microbial biomass (50–80%), while heterotrophic bacterial abundances remained unchanged, and bacterial production rapidly increased (maximal 1,600%, crude-oil > gas-cindensate). These effects were prolonged and lasted several months post hydrocarbons addition, highlighting the sediments as a repository for oil contaminants. Amplicon sequencing of the 16S rRNA gene revealed hydrocarbonoclastic bacteria including Methylophaga, Ponticaulis and Alcanivorax genera post crude-oil addition and Actinobacterota 67–14 lineage following gas-condensate amendments. Our results may enable applying a better science-based environmental policy for the benthic marine environment.

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Response of oligotrophic coastal microbial populations in the SE Mediterranean Sea to crude oil pollution; lessons from mesocosm studies

Cited by 18 publications

References 65 publications

Responses to organic pollutants in the tropical Pacific and subtropical Atlantic Oceans by pelagic marine bacteria

Responses to organic pollutants in the tropical Pacific and subtropical Atlantic Oceans by pelagic marine bacteria

Identification of bacteria in potential mutualism with toxic Alexandrium catenella in Chilean Patagonian fjords by in vitro and field monitoring

Effects of crude oil and gas condensate spill on coastal benthic microbial populations

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