Oil Biodegradation and Bioremediation in Cold Marine Environment

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 21716

Special Issue Editor

Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia
Interests: comparative metagenomic analysis of oil-degrading marine microbiome; development and application of environmental biotechnology for treatment of polluted soil and water
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Special Issue Information

Dear Colleagues,

Petroleum hydrocarbons are released into the marine environment from anthropogenic activities like the drilling, manufacturing, storing, and transporting of crude oil and oil products.  Due to climate change which opens up new shipping routes in the Arctic, there is an increased risk of oil spills due to oil and gas exploration and increased marine traffic in this area. Oil biodegradation in the marine environment is mediated by microbial consortia operating in cooperative metabolic networks, in which a particular microbial species is capable of degrading a certain crude oil components and the product of one oxidation process fuels another. The response of the microbial community to an oil spill at sea is dependent on oil composition and environmental conditions. There is evidence of oil biodegradation occurring at low and sub-zero temperatures but information about to what extent and which microorganisms are involved/contribute to the biodegradation process in the cold marine environment is still scarce. Due to the abovementioned reasons, there is an increased need for more information on the microbial community capacity to degrade oil compounds at taxonomic, functional and genomic levels in the cold marine environment. Recent advances in molecular and data analysis methods allow using multiple sources of information derived from different omic technologies for providing a better understanding of marine microbial community taxonomic and functional structure and its association with oil exposure and oil biodegradation activity. The obtained information enables better predictions for intrinsic biodegradation capacity of oil fractions in seawater, sediments and coastal material and allows assessing and developing specific mitigation approaches for the prevention of negative impact of oil pollution on important ecosystem functions such as nutrient cycling and hypolimnion hypoxia in the cold marine environment.

This Special Issue will publish papers that address: (1) microbial community and metabolic pathways responsible for the degradation of different oil fractions in different marine compartments of the cold marine environment (2) microbial capacity at the taxonomic, functional and genomic levels to respond to and degrade hydrocarbons resulting from the oil spill in the cold marine environment (3) development and application of bioremediation approaches for marine oil spill response in the cold climate and ice-infested areas

Prof. Jaak Truu
Guest Editor

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Keywords

  • Oil biodegradation
  • Oil bioremediation
  • Microbial community
  • Marine environment
  • Arctic
  • Oil pollution

Published Papers (8 papers)

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Editorial

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3 pages, 181 KiB  
Editorial
Oil Biodegradation and Bioremediation in Cold Marine Environment
by Jaak Truu
Microorganisms 2023, 11(5), 1120; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11051120 - 25 Apr 2023
Cited by 1 | Viewed by 929
Abstract
Petroleum hydrocarbons pose a substantial threat to marine ecosystems [...] Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)

Research

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24 pages, 6075 KiB  
Article
Assessment of Hydrocarbon Degradation Potential in Microbial Communities in Arctic Sea Ice
by Angela Peeb, Nga Phuong Dang, Marika Truu, Hiie Nõlvak, Chris Petrich and Jaak Truu
Microorganisms 2022, 10(2), 328; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10020328 - 01 Feb 2022
Cited by 11 | Viewed by 2447
Abstract
The anthropogenic release of oil hydrocarbons into the cold marine environment is an increasing concern due to the elevated usage of sea routes and the exploration of new oil drilling sites in Arctic areas. The aim of this study was to evaluate prokaryotic [...] Read more.
The anthropogenic release of oil hydrocarbons into the cold marine environment is an increasing concern due to the elevated usage of sea routes and the exploration of new oil drilling sites in Arctic areas. The aim of this study was to evaluate prokaryotic community structures and the genetic potential of hydrocarbon degradation in the metagenomes of seawater, sea ice, and crude oil encapsulating the sea ice of the Norwegian fjord, Ofotfjorden. Although the results indicated substantial differences between the structure of prokaryotic communities in seawater and sea ice, the crude oil encapsulating sea ice (SIO) showed increased abundances of many genera-containing hydrocarbon-degrading organisms, including Bermanella, Colwellia, and Glaciecola. Although the metagenome of seawater was rich in a variety of hydrocarbon degradation-related functional genes (HDGs) associated with the metabolism of n-alkanes, and mono- and polyaromatic hydrocarbons, most of the normalized gene counts were highest in the clean sea ice metagenome, whereas in SIO, these counts were the lowest. The long-chain alkane degradation gene almA was detected from all the studied metagenomes and its counts exceeded ladA and alkB counts in both sea ice metagenomes. In addition, almA was related to the most diverse group of prokaryotic genera. Almost all 18 good- and high-quality metagenome-assembled genomes (MAGs) had diverse HDGs profiles. The MAGs recovered from the SIO metagenome belonged to the abundant taxa, such as Glaciecola, Bermanella, and Rhodobacteracea, in this environment. The genera associated with HDGs were often previously known as hydrocarbon-degrading genera. However, a substantial number of new associations, either between already known hydrocarbon-degrading genera and new HDGs or between genera not known to contain hydrocarbon degraders and multiple HDGs, were found. The superimposition of the results of comparing HDG associations with taxonomy, the HDG profiles of MAGs, and the full genomes of organisms in the KEGG database suggest that the found relationships need further investigation and verification. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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23 pages, 6683 KiB  
Article
Microbial Community Dynamics during Biodegradation of Crude Oil and Its Response to Biostimulation in Svalbard Seawater at Low Temperature
by Hiie Nõlvak, Nga Phuong Dang, Marika Truu, Angela Peeb, Kertu Tiirik, Megan O’Sadnick and Jaak Truu
Microorganisms 2021, 9(12), 2425; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9122425 - 24 Nov 2021
Cited by 16 | Viewed by 3479
Abstract
The development of oil exploration activities and an increase in shipping in Arctic areas have increased the risk of oil spills in this cold marine environment. The objective of this experimental study was to assess the effect of biostimulation on microbial community abundance, [...] Read more.
The development of oil exploration activities and an increase in shipping in Arctic areas have increased the risk of oil spills in this cold marine environment. The objective of this experimental study was to assess the effect of biostimulation on microbial community abundance, structure, dynamics, and metabolic potential for oil hydrocarbon degradation in oil-contaminated Arctic seawater. The combination of amplicon-based and shotgun sequencing, together with the integration of genome-resolved metagenomics and omics data, was applied to assess microbial community structure and metabolic properties in naphthenic crude oil-amended microcosms. The comparison of estimates for oil-degrading microbial taxa obtained with different sequencing and taxonomic assignment methods showed substantial discrepancies between applied methods. Consequently, the data acquired with different methods was integrated for the analysis of microbial community structure, and amended with quantitative PCR, producing a more objective description of microbial community dynamics and evaluation of the effect of biostimulation on particular microbial taxa. Implementing biostimulation of the seawater microbial community with the addition of nutrients resulted in substantially elevated prokaryotic community abundance (103-fold), a distinctly different bacterial community structure from that in the initial seawater, 1.3-fold elevation in the normalized abundance of hydrocarbon degradation genes, and 12% enhancement of crude oil biodegradation. The bacterial communities in biostimulated microcosms after four months of incubation were dominated by Gammaproteobacterial genera Pseudomonas, Marinomonas, and Oleispira, which were succeeded by Cycloclasticus and Paraperlucidibaca after eight months of incubation. The majority of 195 compiled good-quality metagenome-assembled genomes (MAGs) exhibited diverse hydrocarbon degradation gene profiles. The results reveal that biostimulation with nutrients promotes naphthenic oil degradation in Arctic seawater, but this strategy alone might not be sufficient to effectively achieve bioremediation goals within a reasonable timeframe. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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19 pages, 1304 KiB  
Article
Diversity and Hydrocarbon-Degrading Potential of Deep-Sea Microbial Community from the Mid-Atlantic Ridge, South of the Azores (North Atlantic Ocean)
by Maria Paola Tomasino, Mariana Aparício, Inês Ribeiro, Filipa Santos, Miguel Caetano, C. Marisa R. Almeida, Maria de Fátima Carvalho and Ana P. Mucha
Microorganisms 2021, 9(11), 2389; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9112389 - 19 Nov 2021
Cited by 7 | Viewed by 3245 | Correction
Abstract
Deep-sea sediments (DSS) are one of the largest biotopes on Earth and host a surprisingly diverse microbial community. The harsh conditions of this cold environment lower the rate of natural attenuation, allowing the petroleum pollutants to persist for a long time in deep [...] Read more.
Deep-sea sediments (DSS) are one of the largest biotopes on Earth and host a surprisingly diverse microbial community. The harsh conditions of this cold environment lower the rate of natural attenuation, allowing the petroleum pollutants to persist for a long time in deep marine sediments raising problematic environmental concerns. The present work aims to contribute to the study of DSS microbial resources as biotechnological tools for bioremediation of petroleum hydrocarbon polluted environments. Four deep-sea sediment samples were collected in the Mid-Atlantic Ridge, south of the Azores (North Atlantic Ocean). Their autochthonous microbial diversity was investigated by 16S rRNA metabarcoding analysis. In addition, a total of 26 deep-sea bacteria strains with the ability to utilize crude oil as their sole carbon and energy source were isolated from the DSS samples. Eight of them were selected for a novel hydrocarbonoclastic-bacterial consortium and their potential to degrade petroleum hydrocarbons was tested in a bioremediation experiment. Bioaugmentation treatments (with inoculum pre-grown either in sodium acetate or petroleum) showed an increase in degradation of the hydrocarbons comparatively to natural attenuation. Our results provide new insights into deep-ocean oil spill bioremediation by applying DSS hydrocarbon-degrading consortium in lab-scale microcosm to simulate an oil spill in natural seawater. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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19 pages, 3246 KiB  
Article
Assessment of the Degradation Potential and Genomic Insights towards Phenanthrene by Dietzia psychralcaliphila JI1D
by Janardhan Ausuri, Giovanni Andrea Vitale, Daniela Coppola, Fortunato Palma Esposito, Carmine Buonocore and Donatella de Pascale
Microorganisms 2021, 9(6), 1327; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9061327 - 19 Jun 2021
Cited by 20 | Viewed by 3195
Abstract
Extreme marine environments are potential sources of novel microbial isolations with dynamic metabolic activity. Dietzia psychralcaliphila J1ID was isolated from sediments originated from Deception Island, Antarctica, grown over phenanthrene. This strain was also assessed for its emulsifying activity. In liquid media, Dietzia psychralcaliphila [...] Read more.
Extreme marine environments are potential sources of novel microbial isolations with dynamic metabolic activity. Dietzia psychralcaliphila J1ID was isolated from sediments originated from Deception Island, Antarctica, grown over phenanthrene. This strain was also assessed for its emulsifying activity. In liquid media, Dietzia psychralcaliphila J1ID showed 84.66% degradation of phenanthrene examined with HPLC-PDA. The identification of metabolites by GC-MS combined with its whole genome analysis provided the pathway involved in the degradation process. Whole genome sequencing indicated a genome size of 4,216,480 bp with 3961 annotated genes. The presence of a wide range of monooxygenase and dioxygenase, as well as dehydrogenase catabolic genes provided the genomic basis for the biodegradation. The strain possesses the genetic compartments for a wide range of toxic aromatic compounds, which includes the benABCD and catABC clusters. COG2146, COG4638, and COG0654 through COG analysis confirmed the genes involved in the oxygenation reaction of the hydrocarbons by the strain. Insights into assessing the depletion of phenanthrene throughout the incubation process and the genetic components involved were obtained. This study indicates the degradation potential of the strain, which can also be further expanded to other model polyaromatic hydrocarbons. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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22 pages, 5113 KiB  
Article
Statistical Optimisation of Diesel Biodegradation at Low Temperatures by an Antarctic Marine Bacterial Consortium Isolated from Non-Contaminated Seawater
by Nur Nadhirah Zakaria, Claudio Gomez-Fuentes, Khalilah Abdul Khalil, Peter Convey, Ahmad Fareez Ahmad Roslee, Azham Zulkharnain, Suriana Sabri, Noor Azmi Shaharuddin, Leyla Cárdenas and Siti Aqlima Ahmad
Microorganisms 2021, 9(6), 1213; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9061213 - 03 Jun 2021
Cited by 15 | Viewed by 3677
Abstract
Hydrocarbon pollution is widespread around the globe and, even in the remoteness of Antarctica, the impacts of hydrocarbons from anthropogenic sources are still apparent. Antarctica’s chronically cold temperatures and other extreme environmental conditions reduce the rates of biological processes, including the biodegradation of [...] Read more.
Hydrocarbon pollution is widespread around the globe and, even in the remoteness of Antarctica, the impacts of hydrocarbons from anthropogenic sources are still apparent. Antarctica’s chronically cold temperatures and other extreme environmental conditions reduce the rates of biological processes, including the biodegradation of pollutants. However, the native Antarctic microbial diversity provides a reservoir of cold-adapted microorganisms, some of which have the potential for biodegradation. This study evaluated the diesel hydrocarbon-degrading ability of a psychrotolerant marine bacterial consortium obtained from the coast of the north-west Antarctic Peninsula. The consortium’s growth conditions were optimised using one-factor-at-a-time (OFAT) and statistical response surface methodology (RSM), which identified optimal growth conditions of pH 8.0, 10 °C, 25 ppt NaCl and 1.5 g/L NH4NO3. The predicted model was highly significant and confirmed that the parameters’ salinity, temperature, nitrogen concentration and initial diesel concentration significantly influenced diesel biodegradation. Using the optimised values generated by RSM, a mass reduction of 12.23 mg/mL from the initial 30.518 mg/mL (4% (w/v)) concentration of diesel was achieved within a 6 d incubation period. This study provides further evidence for the presence of native hydrocarbon-degrading bacteria in non-contaminated Antarctic seawater. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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14 pages, 1819 KiB  
Article
Syntrophic Hydrocarbon Degradation in a Decommissioned Off-Shore Subsea Oil Storage Structure
by Adrien Vigneron, Perrine Cruaud, Frederic Ducellier, Ian M. Head and Nicolas Tsesmetzis
Microorganisms 2021, 9(2), 356; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9020356 - 11 Feb 2021
Cited by 8 | Viewed by 2525
Abstract
Over the last decade, metagenomic studies have revealed the impact of oil production on the microbial ecology of petroleum reservoirs. However, despite their fundamental roles in bioremediation of hydrocarbons, biocorrosion, biofouling and hydrogen sulfide production, oil field and oil production infrastructure microbiomes are [...] Read more.
Over the last decade, metagenomic studies have revealed the impact of oil production on the microbial ecology of petroleum reservoirs. However, despite their fundamental roles in bioremediation of hydrocarbons, biocorrosion, biofouling and hydrogen sulfide production, oil field and oil production infrastructure microbiomes are poorly explored. Understanding of microbial activities within oil production facilities is therefore crucial for environmental risk mitigation, most notably during decommissioning. The analysis of the planktonic microbial community from the aqueous phase of a subsea oil-storage structure was conducted. This concrete structure was part of the production platform of the Brent oil field (North Sea), which is currently undergoing decommissioning. Quantification and sequencing of microbial 16S rRNA genes, metagenomic analysis and reconstruction of metagenome assembled genomes (MAGs) revealed a unique microbiome, strongly dominated by organisms related to Dethiosulfatibacter and Cloacimonadetes. Consistent with the hydrocarbon content in the aqueous phase of the structure, a strong potential for degradation of low molecular weight aromatic hydrocarbons was apparent in the microbial community. These degradation pathways were associated with taxonomically diverse microorganisms, including the predominant Dethiosulfatibacter and Cloacimonadetes lineages, expanding the list of potential hydrocarbon degraders. Genes associated with direct and indirect interspecies exchanges (multiheme type-C cytochromes, hydrogenases and formate/acetate metabolism) were widespread in the community, suggesting potential syntrophic hydrocarbon degradation processes in the system. Our results illustrate the importance of genomic data for informing decommissioning strategies in marine environments and reveal that hydrocarbon-degrading community composition and metabolisms in man-made marine structures might differ markedly from natural hydrocarbon-rich marine environments. Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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Other

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1 pages, 197 KiB  
Correction
Correction: Tomasino et al. Diversity and Hydrocarbon-Degrading Potential of Deep-Sea Microbial Community from the Mid-Atlantic Ridge, South of the Azores (North Atlantic Ocean). Microorganisms 2021, 9, 2389
by Maria Paola Tomasino, Mariana Aparício, Inês Ribeiro, Filipa Santos, Miguel Caetano, C. Marisa R. Almeida, Maria de Fátima Carvalho and Ana P. Mucha
Microorganisms 2022, 10(5), 988; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050988 - 09 May 2022
Viewed by 936
Abstract
The authors wish to make the following corrections to this paper [...] Full article
(This article belongs to the Special Issue Oil Biodegradation and Bioremediation in Cold Marine Environment)
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