Bioremediation of Polycyclic Aromatic Hydrocarbons (PAHs) in the Marine Environment
Ayat Bwsha, MPH Student
Environmental Systems and Human Health Program
The marine ecosystem is one of the most critical ecosystems on the planet. It provides humans and society many beneficial services, such as food security, biodiversity, recreation, and scientific research felid (2). Healthy marine ecosystems are paramount to the world’s population that depends intimately on the oceans and coasts for Eco balance. Maintaining the marine ecosystem's habitat quality and ecosystem health is highly significant. However, marine ecosystem overexploitation has exposed the global water to be seriously threatened by intensive human activities, such as industrial effluents and marine chemical spills, that act as disturbance factors of the health of this system which could become vulnerable exposure sites for pollutants such as polycyclic aromatic hydrocarbons (PAHs) compounds.
What Are Polycyclic Aromatic Hydrocarbons (PAHS)?
Chemical structure of the 16 representative polycyclic aromatic hydrocarbons (PAHs) as decided upon by the United States Environmental Protection Agency (US EPA).
Polycyclic aromatic hydrocarbons (PAHs) are nonpolar organic compounds that naturally occur as complex mixtures in the environment. They are characterized by their benzene ring structures.
PAHs are categorized as general environmentally harmful pollutants by the U.S. Agency for Toxic Substances and Disease Registry who has listed seventeen PAHs as having the most significant potential for adverse human health effects (11).
PAHs Toxicity
Among all organic contaminants that generally alter the marine ecosystem, polycyclic aromatic hydrocarbons (PAHs) represent the largest share(1). They are widely detected in the aquatic environment, including water, sediment, fish, and invertebrates. PAHs are receiving serious concern due to their toxicity, not only towards marine animals but also in humans. Due to their hydrophobicity, PAHs dissolve in fat more than in water. PAHs are carried into the organs and tissues to end up in the cells. Then, the metabolism process is initiated, going through several intermediates, causing PAHs to bind to DNA and become carcinogenic (4). The resulting PAH metabolites appear in urine, and by measuring their concentration, scientists can estimate the amounts of PAHs that have entered the human body.
PAH Routes of Exposure
In general, PAHs can be introduced into the human body through different routes of exposure:
Inhalation,
Dermal absorption
Ingestion through contaminated food
PAH Bioaccumulation
PAHs bioaccumulation properties in the aquatic animal play a vital role in this exposure pathway to humans leading to many toxicological effects, including carcinogenicity, the most concerning the toxic impact of PAHs. IARC (International Agency for Research on Cancer) has classified a group of PAHs as probable or possible human carcinogens, and they can cause carcinogenic effects in humans and other animal species (12).
PAHs Exposure in U.S.
PAHs are widespread in the environment, and its toxicity has driven global health concerns. since the 1980s, the U.S. has initiated public health surveillance actions and regulatory measures to monitor and control PAH exposure. (7)
Based on National Health and Nutrition Examination Survey (NHANES) data to evaluate fourteen-year (2001–2014) urinary PAHs among the non-smoking U.S. population, From 2001 to 02 to 2013–14, some PAHs metabolites concentrations increased in the U.S. general non-smoking population, while other metabolites concentrations decreased over the same time. This study assumed that efforts to reduce PAH exposure did not have uniform effects among non-smoking U.S. residents from 2002 to 2014. (7)
Exposure to Naphthalene and Pyrene increased, while exposure to Fluorene and Phenanthrene decreased among the non-smoking U.S. general population between 2001-2014.
PAHs in the Marine Environment
It is essential to understand contaminants’ bioaccumulation, including its existing factors in a particular environment. Three properties are controlling the PAHs bioavailability in water systems:
Low water solubility,
Less volatility, and
High persistence
Environmental fate and toxic mechanism of aquatic PAHs
Chemical properties tend to make PAHs accumulate in deep sediments, leading to long-term effects on bottom-living organisms (2). And in the tissues of fish and other marine living according to their species-specific fat distribution and habitat location.
Routes of PAH exposures for marine animals and humans
However, it is also important to realize that when sufficiently bioavailable, certain chemicals can produce toxic effects in aquatic organisms and can bioaccumulate in the next level in the food chain due to consumption of those organisms by humans, thereby posing a threat to human health. (9).
PAHs In Seafood
Seafood represents an important and favorable food source for humans that has many nutritional elements and benefits acquired by a rich seafood diet. (6) However, seafood, like other types of food, represents the quality of its environment which can also be a source of harmful environmental contaminants, such as PAHs. (1)
A group of scientists conducted a study to evaluate the possible risks resulting from the ingestion of different seafood species in the Mediterranean Sea. The study examined for the presence of sixteen bioaccumulated PAHs, defined priority by the US-EPA, in two fish species and one shellfish species highly consumed from the local population and caught in the Catania Gulf, an area characterized by high maritime traffic and volcanic activity. (1)
The results showed higher bioaccumulation rates of PAHs in the muscle of the three species related to their fat concentrations. The study claimed that these results were associated with the intense increase in maritime traffic in that area.
Box plot of PAH2, PAH4, PAH8 and PAH16 concentrations in different seafood species
Environmental Justice Issues
“To our communities, being able to fish means being able to either put food on the table or basically eat a much less nutritious meal. I think that’s a non-choice.”
-Audrey Chiang, Asian Pacific Environmental Network, A Seafood Consumption Survey of the Laotian Community in West Contra Costa County, California 1 (1998)
Fisherman in Ghana
While populations and communities worldwide depend differently on the aquatic ecosystems, the impact of the contaminated and depleted marine ecosystems is disproportionately different too. Some communities rely on natural resources of healthy aquatic ecosystems' support in all their lives aspects. Not only for nutritional and economic benefits but also for cultural, traditional, recreational, or religious purposes as well. (13)
Vulnerable communities, such as communities of color, low-income communities, tribes, and other indigenous people, suffer from the accumulated toxins on the aquatic ecosystems with no alternatives to depend on. (13)
Bioremediation as a Ray of Light
The derived PAH to the marine environment undergoes into several natural processes, including adsorption, volatilization, and chemical degradation. Biodegradation by marine microorganisms acts as one of the primary mechanisms to biodegrade/biotransformed the hydrocarbon pollutants, such as PAHs, into less complex metabolites. (15)
Biodegradation refers to the process of transforming or eliminating a chemical compound in the environment involving the living organisms’ biological action. In other words, to be ingested and metabolized by microorganisms. PAHs-degrading microorganisms are widely distributed in the marine environment includes:
Bacteria
Fungi
Algae
Two different mechanisms involve the breakdown of organic compounds through the biodegradation process, which is defined according to the compound location:
1. Aerobic biodegradation on the water surfaces, shorelines, and beaches, where oxygen is available.
2. Anaerobic biodegradation, after sinking in the sediment, where there is no oxygen.
However, biodegradation is a slow process, and the rate of this action depends on different factors to achieve, including the number and type of the microorganisms, nature and chemical structure of the chemical compound being degraded, and the environmental conditions.
Environmental factors affecting marine biodegradation for hydrocarbons are temperature, oxygen, nutrients, and other factors such as pH and salinity. However, the ability to maintain the perfect conditions to accelerate the biodegradation process is the main philosophy behind Bioremediation(8).
Bioremediation is the tool used to optimize the biodegradation process by utilizing the metabolic ability of the microorganisms to enhance the transformation of harmful organic compounds into less harmful or harmless. (8)
Identifying the primary organisms that plays a role in the biodegradation process is vital for developing bioremediation strategies. Therefore, many efforts have been directed to identify and characterize responsible degraders and explore the potential of these degrades.
See mycoremediation for an example of how microorganisms can improve contaminated areas.
Under the Bioremediation umbrella, different bioremediation techniques have been developed to restore polluted environments. Bioremediation techniques are varied depending on their targeted environment and toxin. In marine oil spills, a major source of PAHs contamination, two main techniques/ strategies are used to speed up microbial activities in the hydrocarbons removal process (17):
Biostimulation, Nutrient enrichment.
Bioaugmentation, seeding with naturally occurring microorganisms.
Bioremediation is considered the most effective and clean biodegradation biotechnology in the marine environment to decrease the level of pollution and to recover contaminated marine environments, especially after acute increscent in the PAHs level associated with oil spills.
Bioremediation measures include the amount of nutrients needed to support the microbial requirements for growth, especially after a sudden increase in the hydrocarbon level associated with an oil spill (17). These nutrients, especially nitrogen and phosphorus, act as fertilizers to the contaminated marine environment and stimulate contaminants’ biodegradation.
Bioremediation offers efficient , low-cost, and sustainable PAHs removal approach for the cleanup of polluted marine environments with no conflict with the natural condition.(16)
Protecting Marine Environment, Law & Regulations Examples
EPA’s oil spill prevention program
Includes the Spill Prevention, Control, and Countermeasure (SPCC): "rule helps facilities prevent a discharge of oil into navigable waters or adjoining shorelines" EPA
The Oil Pollution Act (OPA)
"streamlined and strengthened EPA's ability to prevent and respond to catastrophic oil spills. A trust fund financed by a tax on oil is available to clean up spills when the responsible party is incapable or unwilling to do so" EPA
CDC
National Biomonitoring Program: "Biomonitoring data can also help scientists plan and conduct research on exposure and health effects" CDC
United Nations Convention on the Law of the Sea (UNCLOS)
"The law of the sea is a body of public international law governing the geographic jurisdictions of coastal States and the rights and duties among States in the use and conservation of the ocean environment and its natural resources" Encyclopedia of Ocean Sciences (Second Edition), 2001
References
Margherita Ferrante, Guido Zanghì, Antonio Cristaldi, Chiara Copat, Alfina Grasso, Maria Fiore, Santo Salvatore Signorelli, Pietro Zuccarello, Gea Oliveri Conti,PAHs in seafood from the Mediterranean Sea: An exposure risk assessment, Food and Chemical Toxicology, Volume 115, 2018, Pages 385-390, ISSN 0278-6915, https://doi.org/10.1016/j.fct.2018.03.024.
nguo Zhang, Shilan Zhao, Lili Wang, Xiaolong Yang, Qian Zhao, Jingfeng Fan, Xiutang Yuan,Polycyclic aromatic hydrocarbons (PAHs) in seawater and sediments from the northern Liaodong Bay, China,Marine Pollution Bulletin,Volume 113, Issues 1–2,2016,Pages 592-599,ISSN 0025-326X, https://doi.org/10.1016/j.marpolbul.2016.09.005.
Centers for Disease Control and Prevention (April 7, 2017). National Biomonitoring Program. CDC. https://www.cdc.gov/biomonitoring/PAHs_FactSheet.html
Anguo Zhang, Shilan Zhao, Lili Wang, Xiaolong Yang, Qian Zhao, Jingfeng Fan, Xiutang Yuan,Polycyclic aromatic hydrocarbons (PAHs) in seawater and sediments from the northern Liaodong Bay, China, Marine Pollution Bulletin, Volume 113, Issues 1–2, 2016, Pages 592-599, ISSN 0025-326X, https://doi.org/10.1016/j.marpolbul.2016.09.005.
Anguo Zhang, Shilan Zhao, Lili Wang, Xiaolong Yang, Qian Zhao, Jingfeng Fan, Xiutang Yuan, Polycyclic aromatic hydrocarbons (PAHs) in seawater and sediments from the northern Liaodong Bay, China, Marine Pollution Bulletin, Volume 113, Issues 1–2, 2016, Pages 592-599, ISSN 0025-326X, https://doi.org/10.1016/j.marpolbul.2016.09.005.
Naghmeh Soltani, Farid Moore, Behnam Keshavarzi, Armin Sorooshian, Reza Javid, Potentially toxic elements (PTEs) and polycyclic aromatic hydrocarbons (PAHs) in fish and prawn in the Persian Gulf, Iran, Ecotoxicology and Environmental Safety, Volume 173, 2019, Pages 251-265, ISSN 0147-6513, https://doi.org/10.1016/j.ecoenv.2019.02.005.
Barbara Hudson-Hanley, Ellen Smit, Adam Branscum, Perry Hystad, Molly L. Kile, Trends in urinary metabolites of polycyclic aromatic hydrocarbons (PAHs) in the non-smoking U.S. population, NHANES 2001–2014, Chemosphere, Volume 276, 2021,130211, 0045-6535, https://doi.org/10.1016/j.chemosphere.2021.130211.
Bijay Kumar Behera, Abhishek Das, Dhruba Jyoti Sarkar, Pabudi Weerathunge, Pranaya Kumar Parida, Basanta Kumar Das, Palanisami Thavamani, Rajesh Ramanathan, Vipul Bansal, Polycyclic Aromatic Hydrocarbons (PAHs) in inland aquatic ecosystems: Perils and remedies through biosensors and bioremediation, Environmental Pollution, Volume 241, 2018, Pages 212-233, ISSN 0269-7491, https://doi.org/10.1016/j.envpol.2018.05.016.
EPA, Bioaccumulation Testing and Interpretation for the Purpose of Sediment Quality Assessment, Status and Needs, 2000, https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=20003TM1.txt
Illinois Department of Public Health, Division of Environmental Health http://www.idph.state.il.us/cancer/factsheets/polycyclicaromatichydrocarbons.htm
Environmental Health: From Global to Local, 3rd Edition
Federal Advisory Committee to the U.S. Environmental Protection Agency, FISH CONSUMPTION AND ENVIRONMENTAL JUSTICE A Report developed from the National Environmental Justice Advisory Council Meeting of December 3-6, EPA, 2001, https://nepis.epa.gov/Exe/ZyPURL.cgi?Dockey=900A0700.txt
Duran R, Cravo-Laureau C. Role of environmental factors and microorganisms in determining the fate of polycyclic aromatic hydrocarbons in the marine environment. FEMS Microbiol Rev. 2016 Nov 1;40(6):814-830. doi: 10.1093/femsre/fuw031. PMID: 28201512; PMCID: PMC5091036.
A.K. Haritash, C.P. Kaushik, Biodegradation aspects of Polycyclic Aromatic Hydrocarbons (PAHs): A review, Journal of Hazardous Materials, Volume 169, Issues 1–3, 2009, Pages 1-15, ISSN 0304-3894, https://doi.org/10.1016/j.jhazmat.2009.03.137.
Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in Coastal and Marine Environments. J Bioremed Biodeg 6:273. doi:10.4172/2155-6199.1000273
Mehdi Hassanshahian and Simone Cappello (2013) Crude Oil Biodegradation in the Marine Environments, DOI: 10.5772/55554, https://www.intechopen.com/chapters/44369