Introduction

Poly- and perfluoroalkyl substances (PFAS) are a broad range of families of synthetic hydrocarbons that have replaced hydrogen atoms with fluorine atoms in their alkyl chain. This structure has created unique properties in these materials (Kah et al., 2020; Lu et al., 2020). Perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) are the most well-known PFASs, which have been repeatedly detected in various environmental compartments (Abunada et al., 2020). The unique properties of PFAS-containing products are film-forming, water-proof, oil-proof, stain-proof, and low friction. These materials also have excellent water solubility with low reactivity of their carbon–fluorine bond (Yamashita et al., 2008). They are also highly resistant and almost not degraded in the environment; therefore, many scientists called them “forever chemicals” (Pelch et al., 2019). These distinguishing features have made PFAS useful in producing various consumer products since the 1950s (Gardener et al., 2020). Food packaging, Teflon cookware, firefighting foams, carpets, cosmetics, personal care products, glass, paper, stain-proof textile, plastics articles, paints, rust inhibitors, electronics, ski wax, polishers, pesticides, aqueous film-forming foams (AFFF), medical products such as personal protective equipment (PPE), and hundreds of daily goods are examples of consumer products containing PFAS (Cui et al., 2020; Kwiatkowski et al., 2020; Le et al., 2020). PFASs are detected in surface-water, tap water, groundwater, soil, pole, indoor and outdoor air, human plasma, bird, sediment, and ocean, as well as aquatic food webs (Al Amin et al., 2020). For instance, it is reported that the average value of ∑10PFASs concentrations in groundwater in the alluvial–pluvial plain of in the North China Plain is about 2.35 ng/L (Liu et al., 2019). Moreover, the total concentrations of eight quantifiable PFAS (∑8PFAS) in surface waters of the Western Tropical Atlantic Ocean ranged from 11 to 69 pg/L (Han et al., 2022). Similarly, total PFAS mass concentration in the rainwater of eight National Trends Network sites across Wisconsin was between 0.7 and 6.1 ng/L with a median of 1.5 ng/L (Pfotenhauer et al., 2022). Further, according Barghi et al. (2018), median concentration of PFASs in the liver tissues of 10 Korean bird species was 294 ng/g wet weight. Furthermore, Wang et al. (2022) noted that PFAS concentration in sediment, water, muscle and liver tissues of fish in Jiulong River in the southeast of China, ranged from 0.24–1.9 ng g − 1 dw, 2.5 to 410 ng L − 1, 25–100 and 35–1100 ng g − 1 ww, respectively. Persistence, toxicity, and inherent tendency of PFAS to bioaccumulation made them a serious threat to all ecosystems (González-Gaya et al., 2019). Recently, scientists have turned their attention to the presence of PFAS in different depths of the ocean. The concentration of PFAS in the ocean, which has been detected so far, is about several thousand nanograms per liter. However, after firefighting activities, in groundwater and surface water, PFAS with higher concentrations (about mg/L) has also been observed (Abunada et al., 2020). Furthermore, it is expected to significantly increase PFAS concentrations in the ocean in the near future. This is especially true after the COVID-19 pandemic due to the increasing consumption of PFAs containing products, including food packaging, personal care products, single-use plastics, disinfectants, and medical products such as PPEs. As a result, significant amounts of PFAS enter various environment segments and eventually enter the oceans through dust, glacial sediment, storm water and continental shelf remobilization (Fig. 1). When concentrations of PFAS increase in the ocean, they may be ingested at a higher rate than excreted, resulting bioaccumulation. As these compounds are mostly lipophilic (which tend to dissolved in fat rather than water), they could be magnified up through the food web (biomagnification) and enriched in the top of ecosystem (fishes, marine mammals, sea birds, humans) most (Du et al., 2021). In this way, various scientists have pointed to the adverse effects of PFAS on both human and animal health (DeLuca et al., 2021; Fenton et al., 2021; Teunen et al., 2021).

Fig. 1
figure 1

Ocean carbon sequestration process. POC is particulate organic carbon; DOC is dissolved organic carbon; LPOC is labile dissolved organic carbon, and ROPC represents recalcitrant dissolved organic carbon. PFAS can threaten the development of phytoplankton and zooplankton; therefore, ocean PFAS pollution can disrupt carbon sequestration

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Carbon is called the chemical backbone of life on the planet. Carbon compounds regulate the planet’s temperature, make up the food that sustains us and supply energy that fuels our universal economy. The earth’s largest carbon reservoir is rocks and sediments, followed by the ocean, atmosphere, and living organisms. The carbon cycle is defined as carbon flows between different reservoirs in an exchange. As the earth is a closed system, the total quantity of carbon on the planet is constant. However, carbon transferring from one reservoir to another can change the carbon quantity in a specific reservoir. For example, changes that increase the atmosphere’s carbon level visibly contribute to global warming and climate change (Zhu et al., 2019).

The global oceans contain approximately 38,000 gigaton carbon, which is about 45 times more than atmospheric carbon. Moreover, it is estimated that nearly 40% of anthropogenic carbon emissions have already been consumed by oceanic uptake. Thus, global oceans play a prominent role in mitigating atmospheric carbon and maintaining a stable climate. It is even mentioned that in long timescales (more than 100 ka), the ocean and weathering will lessen the level of atmospheric carbon to values near preindustrial (Renforth & Henderson, 2017). But when the oceans’ carbon sequestration ability is disrupted, the global carbon cycle pattern will significantly change. Consequently, the primary conditions for human survival will be treated.

Yet, to our knowledge, there are no scientific studies that evaluate the role of PFAS in disturbing ocean carbon sequestration (OCS). To address this knowledge gap, the present study outlines the existing literature on PFAS and ocean ecosystem interactions to show (1) the effect of PFAS pollution on phytoplankton photosynthesis and growth, (2) the toxic effects of PFAS pollution on the development and reproduction of zooplankton, (3) the effect of PFAS pollution on the marine biological pump, and (4) ocean carbon stock. Moreover, this study has presented some appropriate strategies to address this issue as a complex problem.

Role of ocean PFAS pollution in disrupting OCS

The adverse effect of oceanic PFAS pollution on phytoplankton

As critical primary producers in marine ecosystems, phytoplankton is vital to the stability of the marine ecosystem’s productivity and ecological balance to consume adsorbed carbon from the atmosphere for producing O2 and organic matters by photosynthesis. It implies that phytoplankton supply nutritious food for primary consumers of the ocean (Fig. 1). Therefore, they are known as the foundation of the food web in aquatic ecosystems (Shen et al., 2020). However, marine PFAS pollution can be harmful to photosynthesis and the growth of phytoplankton. Increasing levels of PFAS in marine environments may adversely affect the transmission of sunlight to phytoplankton. Moreover, if PFAS is present in water, it may combine with phytoplankton and prevent sufficient light from reaching the phytoplankton, thereby threatening the photosynthesis of marine primary producers. Furthermore, the toxicity of PFAS can be a significant problem for feeding, growing, metabolism, reproduction, and development of phytoplankton, leading to change in the phytoplankton community. Consequently, threatening the aquatic environment’s stability.

Today the bioaccumulation of PFASs in phytoplankton of the oligotrophic global oceans is reported (Casal et al., 2017). In this way, Table 1 shows the total concentration of PFASs and bioaccumulation factors (BAFs) for various forms of PFAS within oceanic planktons in different aquatic ecosystems. Adverse effects of PFAS on the biological conditions of phytoplankton have been investigated in multiple studies. Zhiguang Niu et al. showed that all three PFAS concentration levels (10 ng L−1, 100 ng L−1, 1000 ng L−1) dramatically inhibited the growth of Chlorella sp. after 14 days (Niu et al., 2019). Wei Liu et al. also reported that Chlorinated poly-fluoroalkyl ether sulfonate (Cl-PFESA) at the levels of mg L−1 concentrations induced harmful impact on the growth, chlorophyll contents, membrane permeability, and level of reactive oxygen species (ROS) in Scenedesmus obliquus (W. Liu et al., 2018). Further, a recent study conducted by Yanyao Li et al. investigated PFOA and its substituent GenX effect on Chlorella pyrenoidosa. They treated C. pyrenoidosa with two concentrations of PFOA and GenX (100 ng L−1 and 100 μg L−1). Their results indicated that after 6 days of treating with these two concentrations of PFOA and GenX, the growth of C. pyrenoidosa began to stop. Moreover, they reported that these two chemicals adversely affect the content of Chlorophyll and the photosynthesis activity of C. pyrenoidosa (Li et al., 2021). The widespread presence of PFAS in the oceans and their bioaccumulation in phytoplankton has been confirmed. Thus, it can be inferred that marine PFASs pollution poses a significant threat to phytoplankton’s growth and reproduction as the vital primary producers of aquatic life, which could eventually disrupt the carbon cycle of the oceans and contribute to global warming and climate change.

Table 1 BAFs (L kg−1) for different forms of PFAS and the concentration of total PFASs in oceanic planktons (ng/g WW)
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The harmful effect of oceanic PFAS pollution on zooplankton

The pelagic food web has a crucial role in controlling the interchange of carbon between the atmosphere and the surface ocean and transferring organic carbon into the ocean floor (Steinberg & Landry, 2017). Within this food web, zooplankton is known as the marine ecosystem’s engineers; since they build the link between primary production, higher trophic levels (such as fish), and communities of deep-sea (Lebrato et al., 2019). Zooplankton takes energy and organic matter from primary producers (such as phytoplankton) and transfers it to higher tropic levels, up to large predators. Degradation of particulate organic carbon (POC) of the oceans can be affected by zooplankton through respiration. In this way, zooplankton affects the depth of re-mineralization of oceanic POC. Therefore, zooplankton has a prominent role in the carbon sequestration of the ocean (Shen et al., 2020). However, increasing concentrations of PFAS in the oceans may change these conditions because marine PFAS pollution can be a significant threat to their development and reproduction. Today, the presence of PFAS in zooplankton has been observed by researchers (Haukås et al., 2007; Munoz et al., 2019; Pascariello et al., 2019). This is also shown in Table 1. Lazhar Mhadhbi et al. in 2012 showed that increment in concentration of PFAS up to mg/L could inhibit embryogenesis in a primary consumer (the echinoderm Paracentrotus lividus) (Mhadhbi et al., 2012). Moreover, Adrienne J. Bartlett et al. indicate that Hyalella azteca (amiphod) survival, reproduction, and growth dramatically declined during exposure to PFOA (Bartlett et al., 2021). Rebecca J. Mitchell et al. have also investigated toxicity induced by Perfluorinated acids in Hyalella azteca species. They also acknowledged that the toxicity of Perfluorinated acids in Hyalella azteca increases with increasing Perfluorinated acids chain length (Mitchell et al., 2011). Although these results originate from laboratory studies with PFAS concentrations higher than the environment, they still have practical importance. Global crisis such as the COVID-19 pandemic and forest fires have led to the widespread use of PFAS-containing materials (medical products and firefighting, respectively). Thus, it is expected that ocean PFAS levels will increasingly increment in the near future. Based on mentioned points, PFAS in the ocean can cause zooplankton to consume less carbon sequestrated by phytoplankton, partly because zooplankton’s toxicity may reduce zooplankton’s consumption capacity and because PFAS diminish the carbon sequestration capacity of phytoplankton. These conditions adversely affect the ability of ocean for the sequestration of global carbon. Consequently, atmospheric carbon dramatically increases, and the pattern of the global carbon cycle will significantly change.

The detrimental effect of oceanic PFAS pollution on the marine biological pump and microbial pump

In the pelagic systems, the most critical process driving anthropogenic carbon sequestration is the biological pump. In this process, atmospheric CO2 is uptaken through phytoplankton’s photosynthesis in the ocean’s euphotic zone; then, this carbon sequestrates to the ocean floor via sinking POC in the form of fecal pellets aggregates, carcasses, and phytodetritus. These fecal pellets end up on the ocean floor and are eventually buried in the sediment (Wieczorek et al., 2019). Thus, fecal pellets constitute a substantial fraction of the mesopelagic POC fluxes. The efficiency of sinking carbon through zooplankton fecal pellets is affected by several factors, including zooplankton community composition, fecal pellets’ production rate, organic composition, and the degradation rate of fecal pellets (Shen et al., 2020). It is reported that fecal pellets can be broken up and then remineralized by zooplankton and prokaryotes during the sinking, decreasing ocean carbon sequestration efficiency. In contrast, a large portion of fecal pellets can reach the ocean floor if fecal pellets production is relatively high to the zooplankton community’s abundances (Belcher et al., 2017). It can be attributed in part to the nature of the substances that zooplankton ingests. PFAS contaminated fecal pellet may change the flux of carbon to the ocean floor. The study of the role of PFAS on the size and shape of fecal pellets of zooplankton is scarce. However, it can be inferred that decreasing or extending transport times of fecal pellet depending on the quantity, type of PFAS ingested.

In general, the POC buried in the ocean floor is less than 0.1% of primary production formed on the ocean’s surface, while the rest of the existing organic carbon is converted chiefly back to CO2. Nonetheless, the ocean still owns a significant dissolved organic carbon (DOC) pool that forms approximately 95% of the remaining organic carbon. A substantial portion of that DOC is recalcitrant. Microbial carbon pump (MCP) is almost a new concept defined as a microbial process, transmuting liable dissolved organic carbon (LDOC) to recalcitrant dissolved organic carbon (RDOC) through the activity of microorganisms, including heterotrophic, autotrophic, prokaryotic as well as viruses (Jiao & Zheng, 2011). The widespread amount of PFAS in the oceans is expected to have an adverse effect on the ocean microbial function and their community, thereby challenging converting LDOC to RDOC. Elena Cerro Galvez showed a direct impact of PFOA and PFOS exposure on natural Antarctic marine microbial communities’ composition and functionality (Cerro Gálvez, 2019). Clearly, PFASs’ potential effects on fecal pellets’ characteristics to the deep ocean and MCP needs further research, which is an origin of very immediate concern.

The potential impact of PFAS in ocean floor on marine carbon stock

Sediments of the ocean floor are among the vastest and essential carbon reservoirs on the earth; accordingly, they are vital for regulating global warming and climate change. It is reported that less than 1% of the planet’s gross production ends up on the ocean floor. Moreover, the organic carbon buried in the seafloor can remain there for thousands to millions of years if left undisrupted (Atwood et al., 2020). The euphotic zone of the ocean is not the end station of marine PFAS pollution. Vertical transport of PFAS and their oceanic sink has been previously documented in the Atlantic ocean, Pacific ocean, and Indian ocean (González-Gaya et al., 2019). The settlement of PFAS on the ocean floor may affect the circulation of organic substances and nutrients in the seafloor. Therefore, it can influence on global carbon stock of the ocean. Indeed, the behaviors and potential effects of the PFAS aphotic zone are significantly unclear, which warrants attention.

Strategies of management and control

Given the above, PFAS pollution is a universal environmental problem. The damage related to PFAS pollution is not limited to a particular region, and its effects and potential threats are worldwide. Thus, countermeasures to control PFAS pollution require cooperation from all counties around the world. Moreover, it is crucial to acknowledge that the proposed solutions for counteracting PFAS pollution must be sustainable. They should contribute considerably to decrease the occurrence of PFAS in the environment, yet they must be by no means exhaustive. Countermeasures to control and manage the PFAS pollution should fix attention to source control, remediation, and clean-up. These measures are presented in the next section. However, it should be noted that each of these strategies has its advantages and disadvantages, which are summarized in Table 2.

Table 2 Advantages and disadvantages of different strategies of PFAS pollution control
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Improving policies and regulations

Indeed, source control is one of the most important measures to reduce PFAS pollution. The source control of PFAS pollution should be implemented through strengthening legislation and the production, sale, and usage of goods, which may cause PFAS pollution to be proscribed. However, until recently, PFAS have significantly been unregulated at the federal level in the USA. In late 2019, the only specific measure related to PFAS taken by the US Environmental protection agency (EPA) was issuing an advisory concentration for only two kinds of PFAS, namely PFOS and PFOA of 70 ppt in drinking water (Dean et al., 2020). Similarly, PFOS and PFOA have been classified under the Stockholm Convention on Persistent Organic Pollutants (POPs), and as a result, they are restricted by the EU POPs Regulation (Ramírez Carnero et al., 2021). However, it seems that these regulations are insufficient for addressing the PFAS threat; thus, many scientists and environmental activists heavily criticized these regulatory actions; because existing laws are dealing with only two compounds of PFAS. Moreover, they had no enforcement mechanism; besides, they proclaim a maximum PFAS level that is insufficient from environmental health aspects. Given that short-chain PFAS has lower performance than that long-chain PFAS (PFOA and PFOS), which may lead to consuming a larger quantity of PFAS in a specific product, resulting in higher emissions of PFAS. Therefore, due to extending threats of PFAS pollution, the international community requires implementing a severe regulatory framework. International organizations should choose a precise and formal definition for PFAS and regulate them as a class, not individual compounds. Moreover, the application of PFAS should be totally banned by global organizations in all unnecessary applicants, and PFAS applications are necessary and unchangeable. Current regulation governing hazardous materials must be applied to reduce the threat to human health and the environment.

Improving 4R concept (Reduce, Recycle, Reuse, Recover) for PFAS containing material

Suppose public awareness of PFAS environmental health risks is widely disseminated through the mainstream media, Big Tech companies. In that case, it can be hoped that consumption of PFAS-containing products (such as Teflon containers) will be significantly reduced. Improving recycling technology, increasing investment in solid waste infrastructure related to recycling, and developing a circular economy can dramatically reduce the amount of PFAS pollution entering the rivers and ocean and, therefore, diminish the rate of PFAS accumulation. Moreover, multiple usages of products that contain PFAS (considering health considerations) can considerably decrease PFAS entering the environment. Usage of PFAS containing products as an energy source and recovery of PFAS containing materials as valuable products and synthetic crude will also be recommended to reduce the entry of PFAS into the environment.

Improving wastewater treatment plant efficiency

Wastewater treatment plants (WWTPs) are the last barrier to PFAS entering the environment. Currently, removal efficiencies for PFAS in most of WWTPs are low (Lenka et al., 2021a). For example, according to the study of Zhang et al. (2013) conducted in China, 16 PFAS were reported in both the influents (between 0.04 and 91 ng/L) and effluents (0.01–107 ng/L) of WWTPs. Thus, existing WWTPs remove only a part of PFAS, and even some studies reported an increase in the concentration of PFAS in the effluent of WWTP compared to influent (Gallen et al., 2018). Researches about remediation techniques at laboratory scale and/or full scale suggest that advanced processes, namely electrochemical degradation, nanofiltration, and adsorption using ion exchange resins, effectively treat PFAS (~ 95–100%) with conventional techniques (Lenka et al., 2021b). However, the applicability of these advanced processes in real-world WWTPs faces many challenges because of mass transfer limitations, the scaling-up requirements, management of treatment by-products, as well as costs. Also, since a significant portion of PFAS enters the sludge of WWTPs, developing and upgrading the sludge treatment facilities in the WWTPs is a necessary step to prevent PFAS from entering the environment.

Improving clean-up and biodegradation technology

Bioremediation uses a biological agent (microorganisms and plants) to degrade and/or accumulate contaminants. This method can be known as a sustainable and cost-effective technique for treating PFAS-contaminated environments. There are known bacteria (primarily identified as Pseudomonas sp.) breaking down the strong F–C bound in PFAS in aerobic and anaerobic conditions (Shahsavari et al., 2020). For instance, it is reported that Pseudomonas parafulva can remove about 32% of PFAS within 96 h of incubation (Yi et al., 2016). Further, a decrease of around 67% in PFAS concentration was also reported during 48 h incubation of Pseudomonas aeruginosa (Kwon et al., 2014). Moreover, Because of the broad range of substrate reduction catalyzed by extracellular ligninolytic enzymes, study on the fungal degradation of PFASs has been ongoing. For example, it is reported that white-rot fungus Phanaerochete chrysosporium can significantly decrease (45%) PFAS concentration for 35 days (Kucharzyk et al., 2017). However, future researches on the implication of fungal enzymes for PFAS treatment seems to be necessary.

Conclusion and future prospective

Global oceans are one of the most extensive natural reservoirs for CO2, which have an essential role in the sequestration of atmospheric carbon and regulating climate change. However, presence of some micropollutans such as PFAS can pose a threat on the ocean’s ability to sequestrate atmospheric CO2. The present study showed that marine PFAS pollution could pose a significant threat to ocean carbon sequestration through four inter-connected scientific pieces of evidence. PFAS is used in a wide range of consumer products. As a result, its concentration in the oceans has incremented in the recent years. The high concentrations of PFAS in the ocean can have adverse effects on the growth and photosynthesis of phytoplankton and toxic effects on zooplankton. As a result, affect on marine biological pomp and carbon stock of the global ocean. However, research on oceanic PFAS on OCS is a new subject for research. Many conclusions are still in the hypothetical steps, and there are significant uncertainties in this subject. Therefore, given the substantial role of the oceans in the deposition of atmospheric carbon and the regulation of the earth’s climatic conditions, and the potential impacts of PFAS on OCS, further research is needed to understand the scale and scope of these effects. Further, herein some unanswered questions are presented that should be answered in future researches:

  • How much does the concentration of different PFAS compounds increase in the biotic and abiotic ocean ecosystem in the post-coronavirus pandemic?

  • What is the concentration threshold of PFAS toxicity for different oceanic biota?

  • Is it possible to produce new compounds of PFAS with less toxic effects on marine biota?

  • What is the effect of different concentrations of PFAS on the size and shape of zooplankton fecal pellets?

  • What is the synergistic effect of the co-existence of PFAS with other emerging pollutants such as Quaternary ammonium compounds (QACs) and/or microplastics on the carbon cycle of the oceans? (Given that in addition to PFAS, the concentration of microplastics and QACs in the environment is expected to increase after the COVID-19 pandemic.)

  • What is the best treatment technique for COVID-19 pandemic-induced waste material?

  • What is the best remediation technique for PFAS on an industrial scale?