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Interaction between per- and polyfluoroalkyl substances and microorganisms

Diying Li, Chunxiao Sun, Xia Liu, Yanhui Dai,Jian Zhao

CHINESE SCIENCE BULLETIN-CHINESE(2023)

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Abstract
Per- and polyfluoroalkyl substances (PFASs) are fluorinated substances that contain at least one completely fluorinated methyl or methylene carbon atom (without any H/Cl/Br/I connected to the carbon atom). Because of the excellent thermal stability, high surface activity, lipophobicity and hydrophobicity, they are widely used in different fields such as non-stick coatings, dental floss, and aqueous film-forming foams. PFASs inevitably enter the environments by industrial and domestic emissions, and exist stably in the environment. In recent years, PFASs pollution becomes a global environmental problem. Microorganisms are an indispensable part of the ecosystems, acting as an important participant in the material cycle and energy flow. Both microbial surfaces and PFASs are relatively hydrophobic, and hydrophobic interaction facilitates PFASs to contact microorganisms, which further inhibit their activity. In turn, microorganisms could affect the transformation and fate of PFASs. Therefore, it is of importance to systematically summarize the interaction between PFASs and microorganisms in order to provide critical information for better understanding the environmental risks of PFASs. This review systematically expounded the interaction between PFASs and environmental microorganisms. Firstly, the cytotoxicity of PFASs to bacteria was highlighted. It was found that PFASs could promote the synthesis and release of extracellular polymeric substances (EPS), and affect the composition and structure of EPS, thereby inhibiting the activity of extracellular enzymes or destroying the integrity of biofilm. In addition, hydrophobic interaction promoted the penetration of PFASs to the phospholipid bilayer, increasing the fluidity and permeability of the membrane. Furthermore, the increase of membrane permeability caused bacterial metabolism disorder, which resulted in the excessive production of reactive oxygen species (ROS). Excessive ROS could oxidize unsaturated fatty acids to malondialdehyde (MDA), and induce crosslinking of nucleic acids and lead to DNA damage. Secondly, this review elucidated the impact of PFASs on the microbial communities in the environments. In the soil and freshwater environments, the changes of bacterial abundance are mainly regulated by PFASs concentrations. It is worth noting that PFASs at high concentration (>10 mg/kg) reduced the abundance of bacteria related to soil nitrogen transformation and phosphorus metabolism, thus posing a potential threat to the cycling capacities of soil nitrogen and phosphorus. Additionally, sulfur cycle and nitrification process in freshwater environment are inhibited by high-concentration PFASs (>10 mg/L). In terms of the marine environment, the impact of PFASs on microbial communities was much lower than that of environmental parameters (e.g., nutrient substances and salinity). Finally, the microbial transformation pathway of PFASs was discussed. The biofilm formed by microorganisms and their extracellular secretions could adsorb and transform/degrade PFASs by different reactions (e.g., Feammox, desulfurization and hydrolysis), mediating by extracellular enzymes (e.g., C-SO3- bond lyase, phosphatase and polyurethane enzyme), thus affecting the toxicity and fate of PFASs. Moreover, the challenges and future perspectives were addressed. PFASs in the biofilm could be transferred to the organisms at higher trophic level through the parasitic or predatory food chains. Therefore, the risk of PFASs along the microbe-based food chain should be further investigated. In addition, microorganisms existed in the environments usually in the form of community. Current research on the molecular mechanisms of PFASs on microbial quorum sensing is relatively lacking, and deserves an in-depth investigation. Finally, due to the lack of some metabolite standards and instrument detection limit, there are still unidentified transformation products in the biotransformation pathways of PFASs. The issues highlighted above are suggested to be focused on the further investigations.
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Key words
toxicity,extracellular secretion,oxidative stress,microorganism community structure,biotransformation
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