https://orcid.org/0000-0002-0731-3662
Abstract
Emerging contaminants (ECs) and microbial communities should not be viewed in isolation, but through the One Health perspective. Both ECs and microorganisms lie at the core of this interconnected framework, as they directly influence the health of humans, animals, and the environment.
The interactions between ECs and microbial communities can have profound implications for public health, affecting all three domains. However, these ECs-microorganism interactions remain underexplored, potentially leaving significant public health and ecological risks unrecognized. Therefore, this article seeks to alert the scientific community to the overlooked interactions between ECs and microbial communities, emphasizing the pivotal role these interactions may play in the management of ‘One Health.’
The most extensively studied interaction between ECs and microbial communities is biodegradation. However, other more complex and concerning interactions demand attention, such as the impact of ECs on microbial ecology (disruptions in ecosystem balance affecting nutrient and energy cycles) and the rise and spread of antimicrobial resistance (a growing global health crisis). Although these ECs-microbial interactions had not been extensively studied, there are scientific evidence that ECs impact on microbial communities may be concerning for public health and ecosystem balance.
So, this perspective summarizes the impact of ECs through a One Health lens and underscores the urgent need to understand their influence on microbial communities, while highlighting the key challenges researchers must overcome. Tackling these challenges is vital to mitigate potential long-term consequences for both ecosystems and public health.
This work highlights the critical and often overlooked interactions between ECs and microbial communities within the One Health framework, emphasizing their potential risks to human, animal, and environmental health. The insights presented in this work underscore the urgent need for interdisciplinary research and policy interventions to mitigate long-term ecological and public health consequences. Understanding and managing EC-microbial interactions is essential for safeguarding global health and ensuring sustainable environmental practices.
Introduction
Water contaminated with emerging contaminants (ECs) of anthropogenic origin is a major global concern. Human activities place massive pressure on water bodies and sources, affecting the delicate balance of associated microbiota, with potentially serious public health consequences (Gomes et al. 2020, Wang et al. 2024a). ECs are chemicals or even microorganisms that are not commonly monitored with potential adverse impact on the environment, animals and/or humans. They are found in everyday products we rely on, such as pharmaceuticals, personal care products, pesticides, detergents, plastics, food additives, and packaging. In fact, their presence in the environment has been dictated by human activities, specifically industrialization and the global life style, which mediate environmental pollution patterns. Therefore, reducing the use of ECs-containing products would require a complete overhaul of our current lifestyle, which is highly impractical. These contaminants enter the environment through various channels: (un)metabolized pharmaceuticals and food additives are excreted and end up in sewage; personal care products and detergents run off into residual water systems; pesticides and fertilizers seep into soils; and, residues from packaging materials contaminate landfills, and consequently soils, and groundwater. These examples represent mainly domestic applications, which alone introduce significant levels of ECs into sewage and soils. Industrial activities and intensive agriculture further amplify the levels of ECs in certain regions.
Recognizing this threat, the European Commission recently proposed a new Directive to establish stricter standards for controlling emerging pollutants in surface and groundwater (EPRS 2023). The currently implemented Water Framework Directive (WFD) identifies 45 chemicals as priority substances, including industrial chemicals, pesticides, and metals; 21 of these are designated as priority hazardous substances due to their persistence, bioaccumulation, and toxicity (EPRS 2023). While the WFD has contributed to reducing EU water contamination, the new proposal aims to further reduce anthropogenic pressure on aquatic ecosystems. The new WFD proposal for surface waters includes 23 individual substances as priority substances, such as pharmaceuticals (macrolide antibiotics, estrogenic hormones, carbamazepine, diclofenac, and ibuprofen); industrial chemicals (bisphenol A); metals (silver); and pesticides (triclosan, nicosulfuron, glyphosate, neonicotinoids, and pyrethroids). Additionally, 24 PFAS (per- and polyfluoroalkyl substances) would be added as a group to the list of priority substances. Some substances that no longer pose an EU-wide risk would be removed from the list. A group of 24 PFAS, pharmaceuticals (carbamazepine and sulfamethoxazole), and pesticide metabolites are listed as new concerning pollutants in groundwater (EPRS 2023).
Unfortunately, conventional wastewater treatment plants (WWTPs) are not designed to remove these contaminants effectively. Consequently, treated wastewater (WW) continues to introduce ECs into water bodies. To address the environmental pressure from contaminated WW and enhance water reuse, the new EU directive for WW proposes systematic monitoring of microplastics, PFAS, pharmaceuticals, and antimicrobial resistance (AMR) elements at both the inlets and outlets of urban WWTPs, as well as in the sludge (EC 2022). Similarly, drinking water treatment plants (DWTPs) are unable to eliminate ECs from captured water, resulting in their presence in drinking water (DW). To combat this, the updated Drinking Water Directive dictates the monitoring of PFAS, microplastics, endocrine disruptors (such as bisphenol A), and disinfection by-products, with implementation being required by 2026 (EU 2020, Dettori et al. 2022).
These updated directives aim to provide a direct answer to the possible impacts of diverse ECs on public health. Although at trace concentrations in the environment, some ECs have been related to significant consequences on public health, such as endocrine disruption, allergic and immunologic effects, and the spread and acquisition of AMR over different ecosystems (Gomes et al. 2020).
The continuous exposure of various microbial communities—ranging from human and animal microbiomes to soil and river microorganisms, WWTP active sludge, and DWTP biofilms—to a complex mix of chemicals (the exposome) at varying concentrations presents unknown risks. Microorganisms are highly adaptable, and exposure to ECs could significantly alter their behaviour and function, posing a serious concern (Gomes et al. 2020). However, research on the impact of ECs on environmental microbial communities remains scarce. Most studies have focused on antibiotics and pharmaceuticals, particularly in fluvial biofilms and activated sludge. The effects of ECs on drinking water microbial communities are even less understood, and the role of non-pharmaceutical ECs, such as personal care products, has been largely overlooked from a ‘One-Health’ perspective. Therefore, this article aims to alert the scientific community to the interactions of ECs with microbial communities and raise awareness about the central role that these ECs—microbial interactions may pose on ‘One-Health’ management.
Emerging contaminants: sources and pathways
ECs are compounds that were initially considered safe and extensively used, often developed as safer and more effective alternatives to replace substances of concern. One of the earliest examples of ECs discussed by the scientific community is the insecticide DDT (Dichlorodiphenyltrichloroethane). DDT was introduced as a safer and more efficient alternative for replacing arsenic-based insecticides and quickly became widely used for various purposes. However, by the early 1960s, its concerning environmental impacts began to draw attention within the scientific community (Sauvé and Desrosiers 2014). Later, in the 1970s and 1980s, evidence of DDT’s severe environmental consequences—including the death and decline of bird populations, bioaccumulation (i.e. accumulation of a contaminant in the tissues of a particular organism over time, typically due to direct exposure from the environment), biomagnification (i.e. increasing concentration of a contaminant as it moves up the food chain, meaning organisms at higher trophic levels accumulate greater amounts due to consumption of contaminated preys), and its ability to travel long distances in the atmosphere—combined with its harmful effects on human health, led to its prohibition in many countries worldwide.
Today, similar debates surround other indispensable compounds and products that are considered essential to modern lifestyles but raise significant concerns for environmental and human health. These include (micro)plastics, fire-retardants such as PFAS, preservatives like certain parabens, and pharmaceutical residues, among many others (Gibson et al. 2023). These substances, once recognized as safe and effective, are now subject to scrutiny and regulatory measures due to their far-reaching consequences.
Given the diverse range of compounds classified as ECs, it is evident that their sources and pathways into the environment are equally varied (Fig. 1). Depending on their uses and applications, the primary sources of ECs can be categorized as industrial (e.g. PFAS and plasticizers), agricultural (e.g. pesticides, fertilizers, and pharmaceuticals), and household or commercial (e.g. detergents, cleaning products, personal care products, and pharmaceuticals). Therefore, it is clear that sewage and insufficiently treated WW are significant contributors to the release of ECs into the environment. Many personal care and household products—such as shampoos, soaps, detergents, and disinfectants—ultimately end up in WW during use, where they flow into sewage systems. Improper disposal of products in landfills also leads to soil contamination, as do agricultural practices involving pesticides, fertilizers, and even animal manure, which are directly applied to fields. This soil contamination can result in the leaching of ECs into groundwater (Gomes et al. 2020).
Major sources of ECs to the environment and their pathways. The main sources include (1) industry, (2) agriculture, and (3) urbanization and household/commercial uses. (a) ECs are emitted directly into the atmosphere from industrial processes, agricultural pulverization, and urban areas. Once in the atmosphere, ECs can be transported to other areas via wind or deposited into (b) soils and (c) water bodies through precipitation. (d) Agriculture contributes to EC release in soils through the application of pesticides, fertilizers, and manure, (e) which can leach into groundwater reservoirs and (f) subsequently be transported to surface waters. (g) Daily usage of various products (e.g. detergents, personal care products, and pharmaceuticals) results in their runoff through sewage systems to (h) WWTPs. Incomplete removal of these contaminants during treatment leads to their release into (i) soils (via reuse of activated sludge) and (j) surface waters. Despite the diversity of pathways, EC transport also occurs within ecosystems: (k) evaporation and aerosolization transport ECs from water to the atmosphere; (l) ECs from water bodies may also accumulate in sediments, transporting ECs to soil; (m) humans and animals may also be exposed to ECs from water bodies through water consumption and recreational use. Created in BioRender. Gomes, I. (2025)https://BioRender.com/h36j860.
In addition to these pathways, atmospheric pollution by ECs occurs, primarily through emissions from anthropogenic activities closely linked to urbanization and industrialization (Enyoh et al. 2020).
Given the ubiquity of these ECs in the environment, their huge chemical diversity and the complexity of sources and dissemination pathways will result in the emergence of several challenges in the detection and analysis of ECs. Among the main challenges faced are the complexity of chemical mixtures found in environmental matrices, their trace concentrations, their possible accumulation in biological tissues and also the lack of standard methodologies and reference materials (Li et al. 2024). Moreover, methods to detect and analyse ECs requires high sensitivity and selectivity, guaranteeing that specific ECs may be distinguished among a myriad of other chemical compounds. In recent years, the scientific community has been dedicated to overcoming these challenges by improving the procedures for sample treatment and applying more sophisticated methodologies, as recently reviewed by Li et al. (2024).
Impacts of ECs on the environment, animal, and human health
The One Health perspective emphasizes the vital interconnectedness of people, animals, and the environment as a foundation for achieving optimal global health. ECs significantly affect all three pillars of One Health—environmental, animal, and human health—as illustrated in Fig. 2.
Impacts of ECs on human, animal, and environmental health, the three pillars of the One Health approach. Water is placed at the centre of this model because it is crucial for life and ecosystem health. ECs and microorganisms are also central, highlighting their widespread distribution and impact on ecosystems. Created in BioRender. Gomes, I. (2025)https://BioRender.com/x94k875.
ECs are often resistant to degradation, allowing them to persist in the environment for extended periods. This persistence leads to bioaccumulation, where these contaminants build up in organisms, potentially reaching harmful levels and posing ecotoxicological risks (Wang et al. 2024a). Although environmental exposure occurs at trace concentrations, the toxicological risks to ecosystems are significant (Haglund and Rebryk 2022, Lu et al. 2022, Yang and Lee 2023, Ehsan et al. 2024, Wang et al. 2024c). Indeed, the phenomenon of hormesis has been observed across a wide range of organisms and ECs, demonstrating that low concentrations can stimulate specific biological processes, while higher concentrations can inhibit biological functions (Evgenios et al. 2022, Rix et al. 2022).
Global efforts have been made to manage ECs release into the environment, innovative water treatments have been studied and tested, conventional treatment plants have been adapted, monitoring and analysis technologies have been improved, risk assessment has been implemented, and official entities have been adjusting regulations about monitoring and removing specific ECs from water but also on banning or restricting the use of concerning substances (Li et al. 2024). All these measures are taken based on the possible consequences of these molecules on human, animal, and environmental health. So, they have been essential not only on ECs control but will also have significant repercussions on public health.
Furthermore, the diverse range of molecules present in the environment and their random interactions in complex mixtures add to the uncertainty regarding their effects, whether individually or combined. Thus, it is crucial to broaden the evaluation of EC interactions across a wide array of substances and mixtures, contributing to the mitigation of potential long-term consequences for ecosystems and public health.
Environmental health
ECs are highly mobile within ecosystems, leading to the contamination of all environmental compartments, including air, soil, and water (Fig. 2). While much scientific focus has been on ECs entering aquatic environments through sewage and treated WW, other significant routes into different environmental compartments include volatilization, aerosolization, diffusive exchange, dry and wet deposition, leaching, and runoff (Barroso et al. 2019). Although ECs may originate in a specific area, they can be transported over long distances through air and water streams, adsorption to organic matter, or bioaccumulation in living organisms such as animals, plants, and microbial communities. The identification of ECs in remote regions like the Arctic and Antarctica further demonstrates this mobility, which may be exacerbated by climate changes (Sonne et al. 2021, Hung et al. 2022, Bolan et al. 2024).
ECs, including substances such as PFAS, preservatives, pharmaceuticals, illicit drugs, phthalates, bisphenol A, microplastics, and nanoplastics, have been detected in urban outdoor air at concentrations ranging from picograms to nanograms per cubic meter (Barroso et al. 2019, Sonne et al. 2021, Hung et al. 2022). Inhalation is, therefore, a significant exposure route to these ECs for both humans and animals. These airborne pollutants can travel to distant locations and have been detected in remote areas, where they have been found in snow, air, and even wildlife (Sonne et al. 2021, D’Amico et al. 2024).
Bioaerosols, which can originate from natural sources such as water, soil, and plants or anthropogenic sources like farms, landfills, and WWTPs, have also been classified as concerning ECs affecting air quality globally (Kim et al. 2018, Xie et al. 2021). These aerosols may contain microorganisms or their fragments, toxins, or metabolites, and can adversely affect air quality and pose health risks to humans and animals. Their small size and light weight enable them to travel between environments, contributing to the excessive accumulation of nutrients in the atmosphere—‘air eutrophication’ (Wang et al. 2024a).
ECs also negatively impact water and soil quality due to their ecotoxicological effects and disruption of biogeochemical cycles, as also happen due to other environmental problems (such as eutrophication). For instance, ECs such as microplastics, heavy metals, personal care products, pharmaceuticals, and phthalates can alter benthic communities (Campos et al. 2020, Tamburini et al. 2020, Pitacco et al. 2022, Gobbato et al. 2024). These communities play crucial roles in maintaining aquatic ecosystem balance specifically on organic matter load, oxygenation, and overall chemical equilibrium. Therefore, nutrient cycling and chemical homeostasis may be compromised in aquatic ecosystems due to water pollution and ECs presence. Therefore, ECs in aquatic environments do not only affect water quality but also biota composition. For example: ECs may be related to a decrease in macroinvertebrate species diversity, and cause DNA damage and detrimental effects on fish populations as disruption of endocrine systems of animals which may also result in carcinogenic effects (Duarte et al. 2023, Das et al. 2024, Picinini-Zambelli et al. 2025).
Similarly, in soil, ECs such as microplastics, pharmaceutical, metals, and pesticides can disrupt microbial communities and the activities of decomposers, affecting the biogeochemical cycle and soil nutrient balance (Pagel et al. 2016, Wang et al. 2022, Chen et al. 2024, Wang et al. 2024c). Although in some cases, the mechanism of action of specific ECs is not yet well understood, there are some hypothesis that may explain this consequences. For example, in case of microplastics, some authors defends that these ECs may contribute for alterations on soil carbon turnover or that their presence in the soil can affect the expression of microbial functional genes that encode enzymes involved in carbon cycling. This disruption can lead to decreased soil fertility and negatively impact plant development. Moreover, soil contamination with ECs may also result in their uptake and translocation through plant roots, contributing to their intake by animals and humans and affecting plant germination and development (Maddela et al. 2022).
In summary, the high mobility and ease of transport of ECs across ecosystems and environmental compartments lead to increased exposure for numerous organisms and communities. This widespread exposure complicates the traceability of ECs and our understanding of their global impacts on environmental health.
Animal and human health
Animals and humans are exposed to ECs through various pathways, including inhalation, ingestion of contaminated water and food, and direct skin contact. One of the most concerning consequences of this exposure is the potential for bioaccumulation and biomagnification, leading to increased health risks.
Bioaccumulation occurs when ECs enter the food chain and gradually build up in the tissues of organisms over time. This is particularly evident with lipophilic compounds which accumulate in fatty tissues across various habitats (Oomen et al. 2018). Biomagnification refers to the increasing concentration of these hydrophobic contaminants as they move up the food chain, resulting in significantly higher levels in top predators (Drouillard 2008). This happens because ECs are not easily metabolized by organisms, leading to accumulation at each trophic level. Over time, this can reach harmful concentrations in top predators. Numerous studies have highlighted the biomagnification potential of various contaminants, including flame retardants like PFAS and dechloranes, as well as UV absorbents (Cadena-Aizaga et al. 2020, Haglund and Rebryk 2022, Liang et al. 2022, Mofijur et al. 2024). PFAS, often referred to as ‘forever chemicals,’ are particularly notorious for their persistence in the environment and their ability to bioaccumulate and biomagnify (Brunn et al. 2023). Similarly, organic UV filters such as benzophenone-3, avobenzone, 3-(4-methylbenzylidene) camphor, and octocrylene, along with UV stabilizers like UV531, UV328, UV329, and UV234, have been found accumulating in aquatic wildlife, such as fish, cephalopods, and crustaceans in the Pearl River Estuary in China (Peng et al. 2017). Notably, UV329, UV531, and octocrylene have shown significant biomagnification potential in these ecosystems (Peng et al. 2017).
EC exposure is not limited to wildlife—it also affects humans. Various ECs have been detected in human body fluids, including blood, serum, amniotic fluid, and breast milk, indicating the extent of human exposure and the potential health risks (Taylor et al. 2014, Wemken et al. 2020, Xue et al. 2024). Flame retardants, especially fluorinated and brominated compounds, have been found in human blood and breast milk, raising concerns about their link to various health disorders (Wemken et al. 2020). Additionally, fragrance compounds like lipophilic synthetic musks have been identified in human blood, adipose tissue, and breast milk (Zhang et al. 2011, Taylor et al. 2014). Microplastics, parabens, phenols, and phthalates have been detected in human amniotic fluid, further highlighting the persistent nature of ECs (Bräuner et al. 2022, Xue et al. 2024).
The presence and accumulation of these diverse chemical contaminants in the bodies of both humans and animals can be linked to a range of significant health issues. These include the development of metabolic syndromes, cancer, chronic nervous system diseases (such as Alzheimer and Parkinson), cardiovascular diseases, and reproductive disorders (Wang et al. 2024a). However, the exposure to ECs have also been related to alteration in the immunological systems and the prevalence of allergic reactions. Several studies point that ECs may compromise the function of immune systems and result in severe allergic reaction. This may be the case of PFAS, where childhood exposure may result in low antibodies production in response to vaccination, increasing the risk for infectious diseases. However, contradictory findings also demonstrated that PFAS may increase allergic reactions (asthma and atopic dermatitis). Therefore, the scientific community assumes that the impact of PFAS on allergic reactions remains inconclusive (von Holst et al. 2021, Ehrlich et al. 2023). Some studies also alert for the possible impact of some ECs (such as trichloroethene, bisphenol A, phthalates, and some pesticides) on the development of auto-immune diseases (Khan and Wang 2019, Sharif et al. 2019, Huang et al. 2023, Yuan et al. 2024).
Another concerning impact of some ECs for human and animal health is their contribution to the development and spread of AMR, affecting significantly the severity of acquired infections and required treatments. Details about the interactions of ECs with microbial cells that may result in the spread of AMR are described in section ‘Antimicrobial resistance and tolerance’.
Microbial communities in One Health
Microbial communities are central to maintaining the balance of One Health (Ma et al. 2023), which is why microorganisms are depicted at the centre of the One Health trilogy in Fig. 2. These communities play a crucial role in regulating environmental health through their involvement in the carbon and nitrogen cycles, interactions with plants, and energy flow via the decomposition of primary energy producers into humus (Ma et al. 2023). Consequently, they are integral to nutrient cycling.
In terms of human and animal health, microorganisms are equally vital. The bodies of humans and animals host millions of microorganisms essential for co-metabolism regulation, ensuring healthy functioning. The intestinal, oral, and skin microbiota are crucial for regulating digestive functions, supporting the immune system, producing vitamins, and protecting against pathogens, among other important tasks (Altveş et al. 2020). Despite the essential and positive interactions between microorganisms and their hosts, there are also negative interactions that pose risks to all the pillars of One Health, particularly from microbial pathogens (Ma et al. 2023). These pathogens cause diseases that can compromise host health and life. Indeed, microbial pathogens often span all three pillars of One Health, with many pathogens infecting humans (such as viruses, protozoa, cyanobacteria, and bacteria) originating from environmental sources like water, soil, and animals. Some notable examples of these bacteria include Legionella pneumophila, Mycobacterium avium complex, Vibrio cholerae, Burkholderia cepacia, and Stenotrophomonas maltophilia (from environmental sources/engineered water systems) and Listeria monocytogenes, Salmonella enterica, and Campylobacter spp. (from animal sources) (Ryan et al. 2009, Lebaron et al. 2015). Approximately 60% of all known human infectious diseases are zoonotic, meaning they originate in animals (Ghai and Behravesh 2024). Moreover, microbial communities are at the core of AMR spread among humans, animals, and the environment, posing a serious threat to One Health (Ma et al. 2023).
In summary, microbial communities are influenced by various external factors, and the extensive interactions between humans, animals, and the environment lead to significant interference and interconnectivity among different microbial communities (Fig. 3).
Interactions of microbial communities across the three pillars of One Health. (a) Exposure to human and animal microbial communities can occur through the food chain or direct interactions with animals, such as farming and petting. (b) Human-associated microbial communities and/or pathogens are introduced into the environment via excretion and wastewater, leading to interactions with the biological communities in WWTPs. (c) Treated WW is released into surface waters, where incoming microbial communities may interfere with indigenous microorganisms involved in nutrient and energy cycles. (d) Activated sludge from WWTPs may be used as soil fertilizer, contributing to interactions with natural soil microbiota. (e) Direct interactions between human and water microbial communities can occur during swimming, fishing, and other aquatic activities. These interactions also happen in situations where sewage treatment is absent. (f) Animal microbiome and/or pathogens are released into soil and water environments, often exacerbated by agricultural practices such as using manure for fertilization. The impact of animal microbial communities on soil microbiota may result in alterations in plant development and microbial load. Created in BioRender. Gomes, I. (2025)https://BioRender.com/k20h750.
Interactions among ECs and microbial communities
Microorganisms exhibit a remarkable ability to quickly adapt to their environmental conditions. Consequently, the presence of ECs in the surrounding environment (water sources, soil, water systems…) significantly affects microbial behaviour, particularly their metabolism and defence mechanisms. Research on microbial interactions with ECs often focuses on their metabolic capabilities, such as their potential to degrade these contaminants and offer new bioremediation solutions (Gomes et al. 2020). Other studies explore how ECs alter microbial metabolism and impact the biogeochemical cycle, thus influencing ecosystem balance (Peng et al. 2020, Yang and Lee 2023). A hot topic in this field is also the effect of specific ECs on the spread and acquisition of AMR (Yang and Lee 2023). Understanding the mechanisms through which microorganisms interact with or respond to ECs is crucial for identifying ecological risks, developing bioremediation strategies, and assessing potential public health threats.
However, research on EC-microbial interactions has been limited to specific EC groups and microbial communities. Pharmaceuticals, particularly antibiotics, carbamazepine, and diclofenac, are among the most studied ECs (Gomes et al. 2020). Yet, many other molecules may pose risks and harm ecosystems. Therefore, it is essential to broaden the scope of research on microorganism–EC interactions to include a wider range of molecules and mixtures. This will help mitigate potential long-term consequences for ecosystems and public health.
Ecological function
Microorganisms play crucial roles in nutrient and energy cycles, making them essential for maintaining equilibrium in ecosystems, as previously mentioned. Since microorganisms are present everywhere, they are inevitably affected by pollutants, including ECs, which can lead to alterations in their communities and metabolic capacities. These changes can, in turn, impact both their hosts and the overall ecosystem balance (Hellal et al. 2023).
Injurious effects are among the potential alterations caused by pollutants, promoting cell damage, genetic mutations, and even death (Chen et al. 2024). Additionally, microorganisms can sometimes shift their metabolism to degrade and transform pollutants, offering a positive ecological function (section ‘Biodegradation’). Unfortunately, the transformation products may occasionally have a more detrimental impact on the community and ecosystem than the original contaminants (Hellal et al. 2023).
In fact, there is growing evidence that, even at trace concentrations, ECs are altering microbial communities in aquatic and soil ecosystems as well as in host guts (Świacka et al. 2023, Burgos-Aceves et al. 2024, Ehsan et al. 2024). For instance, Proia et al. (2013) demonstrated that fluvial biofilms translocated from a non-polluted site to one contaminated with pharmaceuticals and pesticides experienced significant functional changes. These included increased autotrophic biomass, heightened peptidase activity, and reduced photosynthetic efficiency and phosphatase activity (Proia et al. 2013). Similarly, studies have shown that PFAS can affect microbial communities. For example, soil contamination with PFAS has been found to increase bacterial richness but reduce diversity due to the stimulation of certain bacterial genera, such as Firmicutes, Acidobacteria, and Actinobacteria, while inhibiting others like Latescibacteria and Chloroflexi (Ehsan et al. 2024). These alterations in microbial diversity and interactions can impair ecosystem balance, underscoring the complex dynamics at play.
Despite significant advances in microbial ecotoxicology and the focus on the impact of ECs, a broader understanding of the ecological implications of the alterations in microbial communities due to ECs exposure remains challenging (Hellal et al. 2023). One reason for this difficulty is that most studies examining the impact of ECs on microbial diversity and interactions are conducted at the laboratory scale, rather than in real-world systems. While laboratory systems allow for replicability and provide precise information about the effects of ECs on specific microorganisms or communities, they often fail to capture the complexity of entire ecosystems. This makes it difficult to predict the consequences of microbial alterations for all organisms and the environment within an ecosystem.
Some studies have attempted to address this gap by conducting in situ research, correlating water pollution with microbial diversity and activity (Burdon et al. 2020, Peng et al. 2020, Valdés et al. 2023, Murrell et al. 2024). For example, a study of 20 Swiss streams evaluated the impact of WWTP effluents (as a source of ECs) on microbial diversity and function, revealing that treated WW introduced multiple stressors to these communities (Burdon et al. 2020). Through the continuous dosing of pre-defined levels of MPs and nutrients to the river water they found that the presence of ECs was associated with reduced richness and significant compositional turnover of microbial communities exposed downstream of the effluent discharge. Another study examined the enzymatic activity of microbial communities in two Cuban rivers, showing that certain pharmaceuticals inhibited protease, phosphatase, and lipase activities which may reflect microbial ability for organic matter degradation (Murrell et al. 2024). Moreover, the same study demonstrated that exposed microbial community has enhanced catalase activity as a response to oxidative stress. Additionally, research on benthic bacterial communities in Chinese rivers found significant alterations correlated with exposure to contaminants like galaxolide, lead, and triclosan (Peng et al. 2020). Specifically, these authors demonstrated that galaxolide is responsible for 17.7% of the variation in benthic bacteria community composition, while lead and triclosan may cause 6% and 6.5% of variation, respectively.
ECs have also been linked to changes in gut microbiota (Burgos-Aceves et al. 2024). Exposure to various pollutants has adversely affected gut microbial structure and function in aquatic animals, resulting in dysbiosis and compromised host health (Burgos-Aceves et al. 2024). For instance, microplastics in aquatic environments have been associated with gut microbiota dysbiosis in animals like crayfish, where the abundance of opportunistic genera increased due to microplastic exposure (Zhang et al. 2022, Guillén-Watson et al. 2023).
Biofilms in DW distribution systems have also been affected by the presence of ECs. Alterations in biofilm microbial community diversity and in their enzymatic activity have been reported in DW biofilms exposed to sulfadiazine and/or ciprofloxacin (Wang et al. 2019). However, the consequences of ECs exposure to DW natural biofilms have not been extensively studied (Gomes et al. 2020). Also, microbial communities from activated sludge in WWTPs are impacted by continuous exposure to high loads of different emerging pollutants (Kraigher et al. 2008, Davids et al. 2017, Djelal et al. 2024). For example, exposure to the antibiotic doxycycline resulted in a negative impact on settleability and correlated with a decrease in bacterial diversity, promoting floc disintegration and the enrichment of bacterial species known to be antibiotic-resistant (Djelal et al. 2024). The presence of ibuprofen may also alter activated sludge composition. Davids et al. (2017) demonstrated that the impact of ibuprofen on the microbial diversity of activated sludge is dependent on ibuprofen concentration. For lower concentrations of ibuprofen, the microbial diversity is reduced but for higher ibuprofen concentrations the microbial diversity is enhanced. Also, the presence of ibuprofen was associated with the increased occurrence of ciprofloxacin-resistant bacteria (Davids et al. 2017).
These examples illustrate the significant impact ECs can have on natural and engineered ecosystems, even at trace concentrations. It is clear that ECs affect microbial diversity and function, posing challenges to ecosystem equilibrium and functionality. Despite the considerable progress made in microbial ecotoxicology in recent years, significant challenges remain such as the lack of in situ studies, the existence of complex ECs mixtures, high variability of environmental conditions, etc. Overcoming these challenges is essential to better understand the impact of ECs on microbial communities and their direct and indirect consequences for entire ecosystems.
Biodegradation
The use of microbial communities for the degradation of ECs in environmental matrices has been extensively studied, with biodegradation being the most thoroughly investigated interaction between microbial cells and ECs (Gomes et al. 2020). Bioremediation, which relies on these microbial processes, has emerged as a promising environmental strategy for pollution control in water and soil decontamination. It is a cost-effective and eco-friendly approach, widely implemented in WWTPs (Alidoosti et al. 2024, Wang et al. 2024a). Three types of microbial degradation can be defined: bioattenuation (where indigenous microbial populations degrade recalcitrant or xenobiotic compounds through their metabolic processes), biostimulation (where nutrients such as nitrogen, carbon, and oxygen are added to a contaminated site to encourage the growth of naturally occurring degrading strains), and bioaugmentation (where specific competent strains or consortia of microorganisms are introduced to the contaminated site) (María et al. 2016, Karishma et al. 2023). Despite the widespread application of these biodegradation techniques, the dynamics of degrading strains in various environments and the intricate relationship between microbial diversity and contaminant bioremediation remain poorly understood (Sun et al. 2024). This is particularly true for the diverse range of ECs, whose complex chemical structures, toxicity, and low concentrations can hinder degradation by microbial communities (Yin et al. 2024).
Understanding how microbial communities adapt their metabolism and behaviour under different conditions, such as eutrophic (high carbon or nutrient concentrations) or oligotrophic (low concentrations of poorly degradable nutrients and organic carbon) environments, is crucial for improving EC biodegradation. Microbial cells utilize different strategies for nutrient concentration and transport, which can be important for the effective breakdown of ECs (Yin et al. 2024). In that way, several studies have demonstrated that the degradation of ECs by microbial communities can be enhanced in the presence of easily biodegradable organic carbon through a process known as co-metabolism (Kassotaki et al. 2016, Chen and Hyman 2023, Yin et al. 2024). This mechanism can be triggered when ECs exhibit structural similarities to compounds that are readily degraded by microorganisms. For instance, the presence of easily biodegradable substrates is essential for activating the enzymes required for the microbial degradation and metabolization of ECs, as seen in cases like sulfamethoxazole degradation by ammonia-oxidizing bacteria or the aerobic co-metabolic degradation of 1,4-dioxane (Kassotaki et al. 2016, Chen and Hyman 2023).
Enzymes play also a pivotal role in the biodegradation of ECs as they are the primary actors in microbial metabolic pathways. Two key groups of enzymes involved are hydrolases and oxidoreductases (Alidoosti et al. 2024). Oxidoreductases, such as laccases and peroxidases, break the chemical bonds of ECs, leading to the oxidation of contaminants into harmless substances. On the other hand, hydrolases utilize water to cleave large molecules into smaller ones. Both types of enzymes are produced by bacteria and fungi and are capable of degrading various concerning ECs, including bisphenol A, pharmaceuticals (e.g. diclofenac, naproxen, morphine, chloramphenicol, and carbamazepine), estrogenic compounds (e.g. estradiol and estrone), and organophosphate pesticides, among others (Alneyadi et al. 2018, Bittencourt et al. 2023).
Extensive research has been conducted on the use of microbial communities for the biodegradation of ECs in various environments, leading to the identification of several strains as potential degraders of specific ECs. For instance, Priestia sp. and Rhodococcus sp., isolated from marine sediments, demonstrated the ability to degrade hydrophobic contaminants, including certain musk fragrances (tonalid and galaxolide) and UV filters (octocrylene and padimate-O) (Turan et al. 2024). Similarly, Bacillus thuringiensis, also from marine sediments, has been identified as a promising degrader of polyaromatic hydrocarbons and pesticides (Ferreira et al. 2016). Many of these effective biodegraders are microorganisms adapted to prolonged exposure to these specific pollutants, allowing them to resist and metabolize environmental contaminants. For example, a bioaugmentation process was developed using a bacterial consortium from a rubber industry WWTP for the removal of 2-mercaptobenzothiazole, a persistent pollutant from the rubber industry. In this process, a bacterial consortium dominated by Pseudomonas spp. and Stenotrophomonas spp. was immobilized and combined with activated sludge, achieving up to 88% removal of this persistent pollutant (Krainara et al. 2023). These are just a few recent examples of relevant degrading strains and consortia. However, a wide range of microorganisms may adapt their metabolism to degrade various pollutants, as reviewed by Sharma et al. (2023). It is important to note that high removal percentages are often achieved through the use of microbial consortia, as each microorganism within the community can play a distinct metabolic role in the degradation process (Krainara et al. 2023, Aguilar-Romero et al. 2024).
AMR and tolerance
AMR is a significant global threat to public health, and addressing its drivers requires a broader perspective beyond clinical settings. Environmental factors play a crucial role in the emergence and spread of AMR across diverse ecosystems. ECs have been increasingly linked to the rise and dissemination of antibiotic resistance, particularly when they facilitate the transfer of antibiotic resistance genes (ARGs) from environmental bacteria to human pathogens through plasmid conjugation. This poses an arduous challenge to public health (Liu et al. 2023).
Most studies on the role of ECs in AMR focus primarily on the selective pressure exerted by antibiotics and other antimicrobial compounds, such as triclosan, triclocarban, antifungal agents, and surfactants (Alderton et al. 2021). However, antibiotics represent only a small fraction of the bioactive ECs contaminating the environment. Recent evidence suggests that non-antimicrobial molecules may also contribute to the spread of AMR in ecosystems (van Hamelsveld et al. 2023). For instance, Liu et al. (2023) demonstrated that PFAS promote the conjugative transfer of a specific AMR plasmid (RP4) within Escherichia coli. The presence of ARGs in air dust microbiomes has been associated with methylparaben (Hartmann et al. 2016) and, in freshwater environments, methylparaben, ethylparaben, propylparaben, and butylparaben have been linked to an increase in microorganisms resistance to tetracycline, sulfamethoxazole, and parabens (Yang and Lee 2023). Additionally, van Hamelsveld et al. (2023) found that exposure to carbamazepine, clotrimazole, diclofenac, fluoxetine, ibuprofen, methylparaben, sodium benzoate, triclosan, and the herbicide formulation Roundup increased plasmid transmission frequency in E. coli conjugation.
Numerous other studies have shown that a wide variety of ECs across different ecosystems can promote shifts in microbial communities, favouring antimicrobial-resistant bacteria (Gomes et al. 2020). For example, Wang et al. (2019) reported that sulfadiazine and ciprofloxacin were associated with an increase in bacteria carrying ARGs in drinking water biofilms. More recently, Brown et al. (2024) confirmed that antibiotics influence the horizontal gene transfer of ARGs, microbial ecology, and microdiversity-level differences in resistance gene fate in activated sludge. Also, AMR spread may occur due to the influence of specific ECs among rivers and gut microbiota (Stedtfeld et al. 2017, Reddy et al. 2022).
The mechanisms underlying AMR induction and acquisition are varied (Fig. 4). The most commonly associated with EC exposure is the induction of efflux pumps, as demonstrated for the exposure to some biocides (benzalkonium chloride, chlorohexidine, triclosan, polyhexamethylene guanidine, etc.), herbicides (atrazine, pyrethrin, glyphosate…), and pharmaceuticals (such as fluoxetine) (Alderton et al. 2021, Wang et al. 2024b). However, other mechanisms may also be triggered by these pollutants, including alterations in membrane structure and composition as well as changes in protein synthesis, both associated to several biocides (benzalkonium chloride, cetylpyridinium chloride, chlorohexidine, and triclosan) (Alderton et al. 2021, Dettori et al. 2022). The mobility of resistance elements—such as plasmids, introns, and ARGs—facilitates the spread of AMR both within and between species, and among pathogenic and non-pathogenic organisms. Horizontal gene transfer can also be promoted by ECs at environmental concentrations, as demonstrated for triclosan, nanoparticles, polyhexamethylene guanidine, and phthalates (Zhang et al. 2019, Lu et al. 2022, Wu et al. 2023, Wang et al. 2024b). Few works already showed that ECs at trace concentrations might also impact bacteria expression of virulence factors, with results varying significantly among bacteria species tested (Al Haj Ishak Al Ali et al. 2023, Pereira et al. 2023, Aulsebrook et al. 2024).
Mechanism that can be involved in AMR acquisition in response to ECs exposure. (a) Induction of efflux pumps; (b) Alterations in membrane composition and structure; (c) Horizontal gene transfer (mobility of resistance elements by vesiculation, conjugation…); (d) Vertical gene transfer; (e) Changes in protein synthesis; and (f) Expression of virulence factors (such as enzymes as lipases, proteases, gelatinases, mucinases…). Created in BioRender. Gomes, I. (2025)https://BioRender.com/n01b788.
Despite recent evidence demonstrating the direct impact of ECs on the promotion and dissemination of AMR, it is essential to recognize that various environmental factors, (temperature, pH, nutrient availability, co-existence of several pollutants…) can also drive alterations in microbial genomes. Consequently, the influence of ECs on AMR spread may differ across ecosystems, as microorganisms are exposed to diverse environmental conditions. This underscores the importance of conducting new studies that assess the impact of ECs on AMR under conditions that closely mimic real-world scenarios, using microbial communities which are representative of the target ecosystems.
Conclusions
The impact of ECs on human, animal, and environmental health is undeniable. A diverse range of ECs is altering ecosystem dynamics, with concerning consequences documented across all three pillars of One Health. As microorganisms serve as a critical link between these pillars (humans, animals, and environment), this work underscores the urgency of studying the effects of ECs on microbial communities. Among the main ECs-microbial interactions studied by the scientific community, the main three identified were on ecological function, biodegradation and AMR. While much attention has been given to microbial biodegradation of ECs, evidence also reveals that ECs are influencing microbial resistance and adaptation to various environments, posing threats to ecosystem equilibrium and human and animal health.
Despite this knowledge, addressing the challenge remains complex. Ecosystems are influenced by numerous dynamic factors—such as temperature, pH, nutrient availability, and the presence of multiple pollutants—which can further modulate the interactions between ECs and microbial communities, amplifying the risks and variability of observed consequences.
Given the compelling evidence of ECs’ disruptive impacts on microbial communities and the potential repercussions for ecosystems and public health, it is clear that ECs are reshaping microbial dynamics in significant ways. However, the scarcity of comprehensive information on this critical issue highlights an urgent need for further research. While there is a considerable body of work on these topics, the variability in the conditions studied and, in the results obtained hinders their interpretation and limits their usefulness as policy-driving information. This work reinforces the need to deepen our understanding of the public health implications arising from the interaction between ECs and microbial communities.
Author contributions
Inês B. Gomes (Conceptualization, Data curation, Formal analysis, Funding acquisition, Writing – original draft, Writing – review & editing)
Conflict of interest
None declared.
Funding
This work was supported by national funds through FCT/MCTES (PIDDAC): LEPABE, UIDB/00511/2020 (DOI: 10.54499/UIDB/00511/2020) and UIDP/00511/2020 (DOI: 10.54499/UIDP/00511/2020) and ALiCE, LA/P/0045/2020 (DOI: 10.54499/LA/P/0045/2020), the project InnovAntiBiofilm (ref. 101.157.363) financed by European Commission (Horizon-Widera 2023-Acess-02/Horizon-CSA) and the Inês B. Gomes contract 2022.06488.CEECIND/CP1733/CT0008 (DOI:10.54499/2022.06488.CEECIND/CP1733/CT0008) provided by FCT.
Data availability
No new data were generated or analysed in support of this research.
