Title: Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column
ABSTRACT Following oil spills in aquatic environments, oil-associated flocculants observed within contaminated waters ultimately lead to the sedimentation of oil as marine oil snow (MOS). To better understand the role of aggregates in hydrocarbon degradation and transport, we experimentally produced a MOS sedimentation event using Gulf of Mexico coastal waters amended with oil or oil plus dispersant. In addition to the formation of MOS, smaller micrometer-scale (10- to 150-μm) microbial aggregates were observed. Visual inspection of these microaggregates revealed that they were most abundant in the oil-amended treatments and frequently associated with oil droplets, linking their formation to the presence of oil. The peak abundance of the microaggregates coincided with the maximum rates of biological hydrocarbon oxidation estimated by the mineralization of 14 C-labeled hexadecane and naphthalene. To elucidate the potential of microaggregates to serve as hot spots for hydrocarbon degradation, we characterized the free-living and aggregate-associated microbial assemblages using 16S rRNA gene sequencing. The microaggregate population was found to be bacterially dominated and enriched with putative hydrocarbon-degrading taxa. Direct observation of some of these taxa using catalyzed reporter deposition fluorescence in situ hybridization confirmed their greater abundance within microaggregates relative to the surrounding seawater. Metagenomic sequencing of these bacteria-oil microaggregates (BOMAs) further supported their community’s capacity to utilize a wide variety of hydrocarbon compounds. Taken together, these data highlight that BOMAs are inherent features in the biological response to oil spills and likely important hot spots for hydrocarbon oxidation in the ocean. IMPORTANCE Vast quantities of oil-associated marine snow (MOS) formed in the water column as part of the natural biological response to the Deepwater Horizon drilling accident. Despite the scale of the event, uncertainty remains about the mechanisms controlling MOS formation and its impact on the environment. In addition to MOS, we observed micrometer-scale (10- to 150-μm) aggregates whose abundance coincided with maximum rates of hydrocarbon degradation and whose composition was dominated by hydrocarbon-degrading bacteria with the genetic potential to metabolize a range of these compounds. This targeted study examining the role of these bacteria-oil microaggregates in hydrocarbon degradation reveals details of this fundamental component of the biological response to oil spills, and with it, alterations to biogeochemical cycling in the ocean. more »« less
Vázquez Rosas Landa, Mirna; De Anda, Valerie; Rohwer, Robin R.; Angelova, Angelina; Waldram, Georgia; Gutierrez, Tony; Baker, Brett J.
(, mSystems)
Mackelprang, Rachel
(Ed.)
Petroleum pollution in the ocean has increased because of rapid population growth and modernization, requiring urgent remediation. Our understanding of the metabolic response of native microbial communities to oil spills is not well understood. Here, we explored the baseline hydrocarbon-degrading communities of a subarctic Atlantic region to uncover the metabolic potential of the bacteria that inhabit the surface and subsurface water. We conducted enrichments with a 13 C-labeled hydrocarbon to capture the fraction of the community actively using the hydrocarbon. We then combined this approach with metagenomics to identify the metabolic potential of this hydrocarbon-degrading community. This revealed previously undescribed uncultured bacteria with unique metabolic mechanisms involved in aerobic hydrocarbon degradation, indicating that temperature may be pivotal in structuring hydrocarbon-degrading baseline communities. Our findings highlight gaps in our understanding of the metabolic complexity of hydrocarbon degradation by native marine microbial communities.
Sieradzki, Ella T.; Morando, Michael; Fuhrman, Jed A.
(, mSystems)
Rappe, Michael S.
(Ed.)
ABSTRACT Bacterial biodegradation is a significant contributor to remineralization of polycyclic aromatic hydrocarbons (PAHs)—toxic and recalcitrant components of crude oil as well as by-products of partial combustion chronically introduced into seawater via atmospheric deposition. The Deepwater Horizon oil spill demonstrated the speed at which a seed PAH-degrading community maintained by chronic inputs responds to acute pollution. We investigated the diversity and functional potential of a similar seed community in the chronically polluted Port of Los Angeles (POLA), using stable isotope probing with naphthalene, deep-sequenced metagenomes, and carbon incorporation rate measurements at the port and in two sites in the San Pedro Channel. We demonstrate the ability of the community of degraders at the POLA to incorporate carbon from naphthalene, leading to a quick shift in microbial community composition to be dominated by the normally rare Colwellia and Cycloclasticus . We show that metagenome-assembled genomes (MAGs) belonged to these naphthalene degraders by matching their 16S-rRNA gene with experimental stable isotope probing data. Surprisingly, we did not find a full PAH degradation pathway in those genomes, even when combining genes from the entire microbial community, leading us to hypothesize that promiscuous dehydrogenases replace canonical naphthalene degradation enzymes in this site. We compared metabolic pathways identified in 29 genomes whose abundance increased in the presence of naphthalene to generate genomic-based recommendations for future optimization of PAH bioremediation at the POLA, e.g., ammonium as opposed to urea, heme or hemoproteins as an iron source, and polar amino acids. IMPORTANCE Oil spills in the marine environment have a devastating effect on marine life and biogeochemical cycles through bioaccumulation of toxic hydrocarbons and oxygen depletion by hydrocarbon-degrading bacteria. Oil-degrading bacteria occur naturally in the ocean, especially where they are supported by chronic inputs of oil or other organic carbon sources, and have a significant role in degradation of oil spills. Polycyclic aromatic hydrocarbons are the most persistent and toxic component of crude oil. Therefore, the bacteria that can break those molecules down are of particular importance. We identified such bacteria at the Port of Los Angeles (POLA), one of the busiest ports worldwide, and characterized their metabolic capabilities. We propose chemical targets based on those analyses to stimulate the activity of these bacteria in case of an oil spill in the Port POLA.
Seeps, spills and other oil pollution introduce hydrocarbons into the ocean. Marine cyanobacteria also produce hydrocarbons from fatty acids, but little is known about the size and turnover of this cyanobacterial hydrocarbon cycle. We report that cyanobacteria in an oligotrophic gyre mainly produce n-pentadecane and that microbial hydrocarbon production exhibits stratification and diel cycling in the sunlit surface ocean. Using chemical and isotopic tracing we find that pentadecane production mainly occurs in the lower euphotic zone. Using a multifaceted approach, we estimate that the global flux of cyanobacteria-produced pentadecane exceeds total oil input in the ocean by 100- to 500-fold. We show that rapid pentadecane consumption sustains a population of pentadecane-degrading bacteria, and possibly archaea. Our findings characterize a microbial hydrocarbon cycle in the open ocean that dwarfs oil input. We hypothesize that cyanobacterial hydrocarbon production selectively primes the ocean’s microbiome with long-chain alkanes whereas degradation of other petroleum hydrocarbons is controlled by factors including proximity to petroleum seepage.
Summary Marine oil spills are catastrophic events that cause massive damage to ecosystems at all trophic levels. While most of the research has focused on carbon‐degrading microorganisms, the potential impacts of hydrocarbons on microbes responsible for nitrification have received far less attention. Nitrifiers are sensitive to hydrocarbon toxicity: ammonia‐oxidizing bacteria and archaea being 100 and 1000 times more sensitive than typical heterotrophs respectively. Field studies have demonstrated the response of nitrifiers to hydrocarbons is highly variable and the loss of nitrification activity in coastal ecosystems can be restored within 1–2 years, which is much shorter than the typical recovery time of whole ecosystems (e.g., up to 20 years). Since the denitrification process is mainly driven by heterotrophs, which are more resistant to hydrocarbon toxicity than nitrifiers, the inhibition of nitrification may slow down the nitrogen turnover and increase ammonia availability, which supports the growth of oil‐degrading heterotrophs and possibly various phototrophs. A better understanding of the ecological response of nitrification is paramount in predicting impacts of oil spills on the nitrogen cycle under oil spill conditions, and in improving current bioremediation practices.
Brock, Melissa L; Tavares-Reager, Joana F; Dong, Jialin; Larkin, Alyse A; Lam, Toan; Pineda, Nataly; Olivares, Christopher I; Mackey, Katherine_R M; Martiny, Adam C
(, Microbiology Spectrum)
Steven, Blaire
(Ed.)
ABSTRACT An oil spill began in October 2021 off the coast of Orange County, California, releasing 24,696 gallons of crude oil into coastal environments. Although oil spills, such as this one, are recurrent accidents along the California coast, no prior studies have been performed to examine the severity of the local bacterial response. A coastal 10-year time series of short-read metagenomes located within the impacted area allowed us to quantify the magnitude and duration of the disturbance relative to natural fluctuations. We found that the largest change in bacterial beta-diversity occurred at the end of October. The change in taxonomic beta-diversity corresponded with an increase in the sulfur-oxidizing cladeCandidatusThioglobus, an increase in the total relative abundance of potential hydrocarbon-degrading bacteria, and an anomalous decline in the picocyanobacteriaSynechococcus. Similarly, changes in function were related to anomalous declines in photosynthetic pathways and anomalous increases in sulfur metabolism pathways as well as aromatic degradation pathways. There was a lagged response in taxonomy and function to peaks in total PAHs. One week after peaks in total PAH concentrations, the largest shifts in taxonomy were observed, and 1 week after the taxonomy shifts were observed, unique functional changes were seen. This response pattern was observed twice during our sampling period, corresponding with the combined effect of resuspended PAHs and increased nutrient concentrations due to physical transport events. Thus, the impact of the spill on bacterial communities was temporally extended and demonstrates the need for continued monitoring for longer than 3 months after initial oil exposure.IMPORTANCEOil spills are common occurrences in waterways, releasing contaminants into the aquatic environment that persist for long periods of time. Bacterial communities are rapid responders to environmental disturbances, such as oil spills. Within bacterial communities, some members will be susceptible to the disturbance caused by crude oil components and will decline in abundance, whereas others will be opportunistic and will be able to use crude oil components for their metabolism. In many cases, when an oil spill occurs, it is difficult to assess the oil spill’s impact because no samples were collected prior to the accident. Here, we examined the bacterial response to the 2021 Orange County oil spill using a 10-year time series that lies within the impacted area. The results presented here are significant because (i) susceptible and opportunistic taxa to oil spills within the coastal California environment are identified and (ii) the magnitude and duration of thein situbacterial response is quantified for the first time.
Achberger, Amanda M., Doyle, Shawn M., Mills, Makeda I., Holmes, Charles P., Quigg, Antonietta, and Sylvan, Jason B. Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column. Retrieved from https://par.nsf.gov/biblio/10320992. mSystems 6.5 Web. doi:10.1128/mSystems.01105-21.
Achberger, Amanda M., Doyle, Shawn M., Mills, Makeda I., Holmes, Charles P., Quigg, Antonietta, & Sylvan, Jason B. Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column. mSystems, 6 (5). Retrieved from https://par.nsf.gov/biblio/10320992. https://doi.org/10.1128/mSystems.01105-21
Achberger, Amanda M., Doyle, Shawn M., Mills, Makeda I., Holmes, Charles P., Quigg, Antonietta, and Sylvan, Jason B.
"Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column". mSystems 6 (5). Country unknown/Code not available. https://doi.org/10.1128/mSystems.01105-21.https://par.nsf.gov/biblio/10320992.
@article{osti_10320992,
place = {Country unknown/Code not available},
title = {Bacteria-Oil Microaggregates Are an Important Mechanism for Hydrocarbon Degradation in the Marine Water Column},
url = {https://par.nsf.gov/biblio/10320992},
DOI = {10.1128/mSystems.01105-21},
abstractNote = {ABSTRACT Following oil spills in aquatic environments, oil-associated flocculants observed within contaminated waters ultimately lead to the sedimentation of oil as marine oil snow (MOS). To better understand the role of aggregates in hydrocarbon degradation and transport, we experimentally produced a MOS sedimentation event using Gulf of Mexico coastal waters amended with oil or oil plus dispersant. In addition to the formation of MOS, smaller micrometer-scale (10- to 150-μm) microbial aggregates were observed. Visual inspection of these microaggregates revealed that they were most abundant in the oil-amended treatments and frequently associated with oil droplets, linking their formation to the presence of oil. The peak abundance of the microaggregates coincided with the maximum rates of biological hydrocarbon oxidation estimated by the mineralization of 14 C-labeled hexadecane and naphthalene. To elucidate the potential of microaggregates to serve as hot spots for hydrocarbon degradation, we characterized the free-living and aggregate-associated microbial assemblages using 16S rRNA gene sequencing. The microaggregate population was found to be bacterially dominated and enriched with putative hydrocarbon-degrading taxa. Direct observation of some of these taxa using catalyzed reporter deposition fluorescence in situ hybridization confirmed their greater abundance within microaggregates relative to the surrounding seawater. Metagenomic sequencing of these bacteria-oil microaggregates (BOMAs) further supported their community’s capacity to utilize a wide variety of hydrocarbon compounds. Taken together, these data highlight that BOMAs are inherent features in the biological response to oil spills and likely important hot spots for hydrocarbon oxidation in the ocean. IMPORTANCE Vast quantities of oil-associated marine snow (MOS) formed in the water column as part of the natural biological response to the Deepwater Horizon drilling accident. Despite the scale of the event, uncertainty remains about the mechanisms controlling MOS formation and its impact on the environment. In addition to MOS, we observed micrometer-scale (10- to 150-μm) aggregates whose abundance coincided with maximum rates of hydrocarbon degradation and whose composition was dominated by hydrocarbon-degrading bacteria with the genetic potential to metabolize a range of these compounds. This targeted study examining the role of these bacteria-oil microaggregates in hydrocarbon degradation reveals details of this fundamental component of the biological response to oil spills, and with it, alterations to biogeochemical cycling in the ocean.},
journal = {mSystems},
volume = {6},
number = {5},
author = {Achberger, Amanda M. and Doyle, Shawn M. and Mills, Makeda I. and Holmes, Charles P. and Quigg, Antonietta and Sylvan, Jason B.},
editor = {Summers, Zarath M.}
}
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