The effects of per- and polyfluoroalkyl substances on environmental and human microorganisms and their potential for bioremediation

PFAS are present in all ecosystems (40–42) and can easily affect microbes native to these systems/habitats, whose major function is to maintain biotic processes such as nutrient cycling, decomposition of organic matter, and biodegradation of pollutants. Considering that microbes have a brief lifecycle and replicate rapidly due to simple genome, they quickly respond to environmental stress through genetic mutations and may be a good model to study PFAS toxicity. (43). Here we detail the effects of PFAS contamination on microbes in different environmental systems.

PFAS have been found in a variety of aquatic systems, from rivers, lakes, and streams to groundwater, municipal sewage, treated drinking water, rainfall, and snow (44, 45). Volatile PFAS and their precursors, such as fluorotelomer carboxylic acids (FTCA), fluorotelomer unsaturated carboxylic acids (FTUCA), fluorotelomer sulphonate (FTSA), and perfluoroalkane sulphonamido acetic acid (FASAA) undergo a metabolic transformation in the atmosphere to produce short-chain PFSA and PFCA that end up in the aquatic environment. These short-chain PFAS are highly reactive with water (48), easily bioaccumulate in the aquatic food chain, and are toxic to many aquatic organisms (such as invertebrates and green algae) (49).

Due to high hydrophobicity, long-chain PFAS often have an even greater potential for bioaccumulation in aqueous environments and organisms (50). They are often released directly into surface waters from fluorine chemical plants or WWTPs (51). In Fuxin, China, the levels of PFOA have been reported to reach up to 524 ng/L in the groundwater and 668 ng/L in the river (52), which is way above the recommended regulatory standards.

Carbon build-ups in aquatic ecosystems contribute substantially to the control of metabolic activities of environmental microbiomes (53) and to the growth of planktonic bacteria and protozoa. However, PFAS reduce the amount of biogenic and total dissolved carbon in water, which adversely affects many microbial communities and nutrient cycling and composition in aquatic habitats (54, 55). PFOS and PFNA have also been reported to biomagnify in the food web of aquatic animals (56).

Exposure to PFAS significantly affects the balance of bacterial population. There are reports of reduced bacterial diversity and drops in the populations of Actinobacteria and Bacteriodetes (57) in favour of Verrucomicrobia, Proteobacteria (58, 59), and Photobacterium phosphoreum in surface water (60, 61). These studies also report that perfluoro butanoic acid (PFBA) interferes with the transfer of nutrients in bacteria (60), while perfluorotetradecanoic acid (PFTeDA) moves up the food chain from heterotrophic bacteria to amoebae (protozoa) (59). Some genera, such as Bacteroidetes, Proteobacteria, and especially Acidobacteria, have been reported resistant to PFAS concentrations of up to 20 mg/L (62) (Table 2).

The molecular mechanism of PFAS toxicity to microbes involves oxidative stress, which damages the cell membrane and DNA, rendering some bacteria inactive (63, 64).

Sediments provide a habitat for a wide variety of benthic organisms, and much of their biomass includes microorganisms important for ecological processes such as biodegradation, biogeochemical cycling, and bioremediation (66–70).

Pollutants such as PFAS seem to have a major role in structuring microbial communities and their function in aquatic sediments (71, 72). Long-chained PFAS tend to build up over time (65, 73), which, once a threshold is crossed, may have irreversible negative effects on microbial populations and the structure of the benthic zone (74–77). In such conditions, tolerant and sulphate-reducing strains like the Desulfococcus genus and GOUTA19, become dominant microbial communities, and diversity drops (77–79).

Reports about the occurrence and toxicity of PFAS in drinking water come from all over the world (28, 48, 80). Average concentrations range between <10 ng/L and 1200 ng/L (81–85). PFAS occurrence in drinking water has been linked to several sources such as nearby fluorochemical production plants, PFAS-based firefighting foam (86), WWTPs, and surface runoff (87). Even at low concentrations (ng/L) PFAS in drinking water may have deleterious effects on human health as PFAS tend to build up in the liver and affect liver function (88). PFAS contamination of drinking water at levels above the United States Environmental Protection Agency (US EPA) health-based reference level of 70 ng/L (89) have also been associated with pregnancy-induced high blood pressure, hypertension, and preeclampsia as well as testicular and kidney cancers. Continued testing of drinking water and implementation of regulatory measures is therefore essential for keeping PFAS concentrations below this limit.

Soil takes the lead as a sink for persistent chemical pollutants released into the environment from sources such as fluoride plants, aqueous film-forming foam from fire training sites, and sludge and biosolids from WWTPs, landfills, and incineration plants (6, 90–92). PFAS accumulate in soil over time and persist there for a long time, affecting micro and macro-organisms, which are abundant and serve to decompose organic matter, recycle biogeochemicals and nutrients, and remediate soil of contaminants (5, 43).

Soils are mostly contaminated by PFOS, because of their widespread and long-time application (94), but all PFAS change the structure of soil and, consequently, the distribution and function of microbial communities (5, 75, 93, 94). A recent study relying on a next generation sequencing technology (95) showed that PFOA in low concentrations affect bacterial diversity in soil less than PFOS. As for PFAS toxicity in soil microbial species, the mechanisms include membrane disruption, oxidative stress, and DNA damage-induced inactivation and/or death in Escherichia coli (96). In Pseudomonas putida PFOA is more toxic when combined with either chromium or tetra butyl ammonium (97).

PFAS contamination usually affects the diversity and composition of soil microbial communities. Long-chained PFAS and PFAS with the sulphonic group are more toxic to soil microbial flora than short-chained PFAS with carboxylic groups (97). There are reports, sometimes apparently controversial, that some important bacterial groups are eliminated, such as Cyanobacteria (75, 78), or depleted, such as Chloroflexi, Haliangium, Latescibacteria, and some species of the genus Acidobacteria (6, 35, 75). Higher PFC concentrations are also known to impede the growth and metabolism of the Bacillus spp. (95) and Sphingomonas paucimobilis (104, 105).

Other groups seem to thrive, such as Firmicutes, some Acidobacteria, and Actinobacteria (75). Comparative studies of bacterial communities affected by PFAS contamination point to potential changes in soil nutrients (5, 97, 98), total carbon, and pH (99). Elevated PFOA concentrations in sediments seem to boost some populations of Proteobacteria (100–102), such as Pseudomonas spp., which may be owed to their ability to defluorinate fluorotelomer alcohols by removing multiple CF2 groups to form shorter-chain PFCAs (102), which are less toxic (95, 103) and quicker to degrade (95). Besides Proteobacteria, Verrucomicrobia also seem to withstand PFAS contamination (106) (Table 2).

Greater abundance of some bacteria in contaminated soils provides an insight into which bacterial groups could be used to enhance PFAS biodegradation and bioremediation.

As PFAS contamination affects the composition and diversity of microorganisms in soil, so does it affect its organic matter content (107, 108). Soil microorganisms are active in biogeochemical cycling and play an important role in pollutant degradation (109). The effect of PFAS on soil microbial populations may therefore affect the microbial diversity and ability to carry out geochemical processes in the soil (109, 110).

PFAS-induced changes in the abundance of fungi and bacteria may reflect on the organic content in soil and eventually carbon content available for cycling. However, possible connections with biogeochemical cycles have not been elucidated yet.

Zhalnina et al. (111) studied the effect of PFAS on the nitrogen cycle (nitrification and denitrification) and related cycle genes in 61 ammonia-oxidising microorganisms and reported that PFAS did not affect the ammonia monooxygenase gene abundance in bacteria but reduced it significantly in archaea. In fact, PFAS treatment seems to have favoured the growth of Acidovorax temperans in the soil. A. temperans is notorious for reducing the nitrate content in soil, and its proliferation implies nitrate depletion in PFAS-contaminated soils (Table 3). In contrast, nitrate- and sulphate-reducing bacterial genera, such as Acidobacteria, and Gammaproteobacteria, are inhibited by PFAS (35), leading to an increase in the level of nitrates and sulphates in the soil (35). Nitrates and sulphate concentrations and pH levels of contaminated soils influence nutrient availability, which, in turn, influences which plants will grow there.

As for the carbon cycle, PFAS are reported to inhibit glycoside hydrolases and interrupt carbohydrate metabolism and membrane transport in soil microbes (99). In addition to glycoside hydrolase inhibition, long-chain PFAS inhibit the activity of sucrase and urease (75).

Several studies have shown that PFAS accumulate in spring wheat, oats, potatoes, maize, perennial ryegrass, winter wheat, winter rye, canola, winter barley, carrots, and cucumber through soil (112–115). The last two studies (114, 115) point to the use of sewage effluent as fertiliser that contaminates the soil and then crops. Lechner and Knapp (114) further discourage the idea of air-to-plant transfer, as plants growing on soil not fertilised by sludge showed no increase in PFAS concentrations.