Characterization of hydrocarbon degraders from Northwest Passage beach sediments and assessment of their ability for bioremediation.

Global warming-induced sea ice loss in the Canadian Northwest Passage (NWP) will result in more shipping traffic, increasing the risk of oil spills. Microorganisms inhabiting NWP beach sediments may degrade hydrocarbons, offering a potential bioremediation strategy. In this study, the characterization and genomic analyses of 22 hydrocarbon-biodegradative bacterial isolates revealed that they contained a diverse range of key alkane and aromatic hydrocarbon-degradative genes, as well as cold and salt tolerance genes indicating they are highly adapted to the extreme Arctic environment. Some isolates successfully degraded Ultra Low Sulfur Fuel Oil (ULSFO) at temperatures as low as -5 °C and high salinities (3%-10%). Three isolates were grown in liquid medium containing ULSFO as sole carbon source over 3 months and variation of hydrocarbon concentration was measured at three time points to determine their rate of hydrocarbon biodegradation. Our results demonstrate that two isolates (Rhodococcus sp. R1B_2T and Pseudarthrobacter sp. R2D_1T) possess complete degradation pathways and can grow on alkane and aromatic components of ULSFO under Arctic conditions. Overall, these results demonstrate that diverse hydrocarbon-degrading microorganisms exist in the NWP beach sediments, offering a potential bioremediation strategy in the events of a marine fuel spill reaching the shores of the NWP.

Long-term biodegradation of crude oil in high-arctic backshore sediments: The Baffin Island Oil Spill (BIOS) after nearly four decades.

With an on-going disproportional warming of the Arctic Ocean and the reduction of the sea ice cover, the risk of an accidental oil spill from ships or future oil exploration is increasing. It is hence important to know how crude oil weathers in this environment and what factors affect oil biodegradation in the Arctic. However, this topic is currently poorly studied. In the 1980s, the Baffin Island Oil Spill (BIOS) project carried out a series of simulated oil spills in the backshore zone of beaches located on Baffin Island in the Canadian High Arctic. In this study two BIOS sites were re-visited, offering the unique opportunity to study the long-term weathering of crude oil under Arctic conditions. Here we show that residual oil remains present at these sites even after almost four decades since the original oiling. Oil at both BIOS sites appears to have attenuated very slowly with estimated loss rates of 1.8-2.7% per year. The presence of residual oil continues to significantly affect sediment microbial communities at the sites as manifested by a significantly decreased diversity, differences in the abundance of microorganisms and an enrichment of putative oil-degrading bacteria in oiled sediments. Reconstructed genomes of putative oil degraders suggest that only a subset is specifically adapted for growth under psychrothermic conditions, further reducing the time for biodegradation during the already short Arctic summers. Altogether, this study shows that crude oil spilled in the Arctic can persist and significantly affect the Arctic ecosystem for a long time, in the order of several decades.

High Arctic seawater and coastal soil microbiome co-occurrence and composition structure and their potential hydrocarbon biodegradation.

The accelerated decline in Arctic sea-ice cover and duration is enabling the opening of Arctic marine passages and improving access to natural resources. The increasing accessibility to navigation and resource exploration and production brings risks of accidental hydrocarbon releases into Arctic waters, posing a major threat to Arctic marine ecosystems where oil may persist for many years, especially in beach sediment. The composition and response of the microbial community to oil contamination on Arctic beaches remain poorly understood. To address this, we analyzed microbial community structure and identified hydrocarbon degradation genes among the Northwest Passage intertidal beach sediments and shoreline seawater from five high Arctic beaches. Our results from 16S/18S rRNA genes, long-read metagenomes, and metagenome-assembled genomes reveal the composition and metabolic capabilities of the hydrocarbon microbial degrader community, as well as tight cross-habitat and cross-kingdom interactions dominated by lineages that are common and often dominant in the polar coastal habitat, but distinct from petroleum hydrocarbon-contaminated sites. In the polar beach sediment habitats, Granulosicoccus sp. and Cyclocasticus sp. were major potential hydrocarbon-degraders, and our metagenomes revealed a small proportion of microalgae and algal viruses possessing key hydrocarbon biodegradative genes. This research demonstrates that Arctic beach sediment and marine microbial communities possess the ability for hydrocarbon natural attenuation. The findings provide new insights into the viral and microalgal communities possessing hydrocarbon degradation genes and might represent an important contribution to the removal of hydrocarbons under harsh environmental conditions in a pristine, cold, and oil-free environment that is threatened by oil spills.

Metagenomic survey reveals hydrocarbon biodegradation potential of Canadian high Arctic beaches.

BACKGROUND: Decreasing sea ice coverage across the Arctic Ocean due to climate change is expected to increase shipping activity through previously inaccessible shipping routes, including the Northwest Passage (NWP). Changing weather conditions typically encountered in the Arctic will still pose a risk for ships which could lead to an accident and the uncontrolled release of hydrocarbons onto NWP shorelines. We performed a metagenomic survey to characterize the microbial communities of various NWP shorelines and to determine whether there is a metabolic potential for hydrocarbon degradation in these microbiomes. RESULTS: We observed taxonomic and functional gene evidence supporting the potential of NWP beach microbes to degrade various types of hydrocarbons. The metagenomic and metagenome-assembled genome (MAG) taxonomy showed that known hydrocarbon-degrading taxa are present in these beaches. Additionally, we detected the presence of biomarker genes of aerobic and anaerobic degradation pathways of alkane and aromatic hydrocarbons along with complete degradation pathways for aerobic alkane degradation. Alkane degradation genes were present in all samples and were also more abundant (33.8 ± 34.5 hits per million genes, HPM) than their aromatic hydrocarbon counterparts (11.7 ± 12.3 HPM). Due to the ubiquity of MAGs from the genus Rhodococcus (23.8% of the MAGs), we compared our MAGs with Rhodococcus genomes from NWP isolates obtained using hydrocarbons as the carbon source to corroborate our results and to develop a pangenome of Arctic Rhodococcus. Our analysis revealed that the biodegradation of alkanes is part of the core pangenome of this genus. We also detected nitrogen and sulfur pathways as additional energy sources and electron donors as well as carbon pathways providing alternative carbon sources. These pathways occur in the absence of hydrocarbons allowing microbes to survive in these nutrient-poor beaches. CONCLUSIONS: Our metagenomic analyses detected the genetic potential for hydrocarbon biodegradation in these NWP shoreline microbiomes. Alkane metabolism was the most prevalent type of hydrocarbon degradation observed in these tidal beach ecosystems. Our results indicate that bioremediation could be used as a cleanup strategy, but the addition of adequate amounts of N and P fertilizers, should be considered to help bacteria overcome the oligotrophic nature of NWP shorelines.

Hydrocarbon bioremediation on Arctic shorelines: Historic perspective and roadway to the future.

Climate change has become one of the greatest concerns of the past few decades. In particular, global warming is a growing threat to the Canadian high Arctic and other polar regions. By the middle of this century, an increase in the annual mean temperature of 1.8 °C-2.7 °C for the Canadian North is predicted. Rising temperatures lead to a significant decrease of the sea ice area covered in the Northwest Passage. As a consequence, a surge of maritime activity in that region increases the risk of hydrocarbon pollution due to accidental fuel spills. In this review, we focus on bioremediation approaches on Arctic shorelines. We summarize historical experimental spill studies conducted at Svalbard, Baffin Island, and the Kerguelen Archipelago, and review contemporary studies that used modern omics techniques in various environments. We discuss how omics approaches can facilitate our understanding of Arctic shoreline bioremediation and identify promising research areas that should be further explored. We conclude that specific environmental conditions strongly alter bioremediation outcomes in Arctic environments and future studies must therefore focus on correlating these diverse parameters with the efficacy of hydrocarbon biodegradation.

Distinct gut microbiomes in two polar bear subpopulations inhabiting different sea ice ecoregions.

Gut microbiomes were analyzed by 16S rRNA gene metabarcoding for polar bears (Ursus maritimus) from the southern Beaufort Sea (SB), where sea ice loss has led to increased use of land-based food resources by bears, and from East Greenland (EG), where persistent sea ice has allowed hunting of ice-associated prey nearly year-round. SB polar bears showed a higher number of total (940 vs. 742) and unique (387 vs. 189) amplicon sequence variants and higher inter-individual variation compared to EG polar bears. Gut microbiome composition differed significantly between the two subpopulations and among sex/age classes, likely driven by diet variation and ontogenetic shifts in the gut microbiome. Dietary tracer analysis using fatty acid signatures for SB polar bears showed that diet explained more intrapopulation variation in gut microbiome composition and diversity than other tested variables, i.e., sex/age class, body condition, and capture year. Substantial differences in the SB gut microbiome relative to EG polar bears, and associations between SB gut microbiome and diet, suggest that the shifting foraging habits of SB polar bears tied to sea ice loss may be altering their gut microbiome, with potential consequences for nutrition and physiology.

Gut microbiome is affected by inter-sexual and inter-seasonal variation in diet for thick-billed murres (Uria lomvia).

The role of the gut microbiome is increasingly being recognized by health scientists and veterinarians, yet its role in wild animals remains understudied. Variations in the gut microbiome could be the result of differential diets among individuals, such as variation between sexes, across seasons, or across reproductive stages. We evaluated the hypothesis that diet alters the avian gut microbiome using stable isotope analysis (SIA) and 16S rRNA gene sequencing. We present the first description of the thick-billed murre (Uria lomvia) fecal microbiome. The murre microbiome was dominated by bacteria from the genus Catellicoccus, ubiquitous in the guts of many seabirds. Microbiome variation was explained by murre diet in terms of proportion of littoral carbon, trophic position, and sulfur isotopes, especially for the classes Actinobacteria, Bacilli, Bacteroidia, Clostridia, Alphaproteobacteria, and Gammaproteobacteria. We also observed differences in the abundance of bacterial genera such as Catellicoccus and Cetobacterium between sexes and reproductive stages. These results are in accordance with behavioural observations of changes in diet between sexes and across the reproductive season. We concluded that the observed variation in the gut microbiome may be caused by individual prey specialization and may also be reinforced by sexual and reproductive stage differences in diet.

Nitrogen and sulfur isotopes predict variation in mercury levels in Arctic seabird prey.

Mercury (Hg) biotransformation and biomagnification are processes that affect Hg burdens in wildlife. To interpret variation in Hg in seabird eggs, used as Hg bioindicators in the Arctic, it is important to understand how Hg biomagnifies through the food web. We evaluated the use of δ34S, along with other commonly used stable isotope signatures (δ15N and δ13C), for the determination of possible sources of Hg in an Arctic food web (56 individuals of 15 species of fish and invertebrates). Hg correlated with δ34S (R2 = 0.72). When the combined effects of δ34S and δ15N were considered in mixed-effects models, both δ34S and δ15N together described Hg patterns in Arctic food webs better than either isotope alone. Our results demonstrate the usefulness of δ34S to account for variation in Hg among marine animals and to study the possible underlying effects that MeHg production may have on Hg pathways in Arctic ecosystems.

Toxic metals and associated sporulated bacteria on Andean hummingbird feathers.

Human activities in the Sabana de Bogotá, Colombia, release toxic metals such as lead (Pb) and chromium (Cr) into the environment polluting the air, water, and soil. Because birds are in contact with these pollutants and their sources, they may serve as bioindicator organisms. We evaluated the use of hummingbird feathers obtained from individuals captured in three sites of the Sabana de Bogotá as bioindicators of toxic metal pollution using spectrophotometric and spectroscopic methods based on single-feather samples. We also characterized the bacterial microbiota associated with hummingbird feathers by molecular identification using the 16S rRNA with a special focus on sporulated bacteria. Finally, we described the interactions which naturally occur among the feathers, their associated bacteria, and pollutants. We found differences in Pb and Cr concentrations between sampling sites, which ranged from 2.11 to 4.69 ppm and 0.38 to 3.00 ppm, respectively. This may reflect the impact of the activities held in those sites which release pollutants to the environment. Bacterial assemblages mainly consisted of sporulated bacilli in the Bacillaceae family (65.7 % of the identified morphotypes). We conclude that the feathers of wild tropical birds, including hummingbirds, can be used as lead and chromium bioindicators and that bacteria growing on feathers may in fact interact with these two toxic metals.