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, 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.
Highlights
IntroductionMarine ecosystems are exposed to petroleum hydrocarbons through a variety of natural mechanisms, such as natural seeps, and anthropogenic activities, such as accidental oil spills during oil production and transport
For the taxonomic assignment of shotgun metagenomic data, numerous classifiers and reference databases are available that fall into several categories: (i) DNA-to-DNA methods, where perfect matches between sequence stretches and reference sequences (k-mers) are sought (e.g., Kraken2, Bracken, and PathSeq); (ii) DNA-to-protein methods, where sequence reads are compared with protein-coding sequences (e.g., Kaiju and DIAMOND); and (iii) DNA-tomarker methods, including only specific marker gene families in reference databases (e.g., MetaPhlAn2) [43,44]
The variations detected in the estimates of bacterial community structure and taxa proportions when comparing several different taxonomic classification methods indicate that for Arctic marine microbial communities, direct comparisons between amplicon-based and metagenome-based methods should be avoided or used with extreme care
Summary
Marine ecosystems are exposed to petroleum hydrocarbons through a variety of natural mechanisms, such as natural seeps, and anthropogenic activities, such as accidental oil spills during oil production and transport. Climate change has elevated the risk of crude oil spillage, especially in cold Arctic marine environments, where the severely reduced sea-ice-covered area has enabled the growth of oil exploration activity as well as prolonged and more frequent usage of Arctic shipping routes [1]. In Arctic regions, the complete clean-up of oil spills using traditional methods such as skimmers or beams. Microorganisms 2021, 9, 2425 is often challenging due to remote or poorly accessible locations and extreme weather conditions [2]. Bioremediation techniques, which rely on the potential of indigenous seawater microbial communities to degrade oil hydrocarbons, have been suggested as suitable and labor-effective clean-up methods in remote Arctic locations
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