Editorial: Microbial Ecotoxicology

Stéphane Pesce, Jean-François Ghiglione, Edward Topp, Fabrice

Martin-Laurent

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Stéphane Pesce, Jean-François Ghiglione, Edward Topp, Fabrice Martin-Laurent. Editorial: Microbial Ecotoxicology. Frontiers in Microbiology, 2020, 11, 10.3389/fmicb.2020.01342. [https://doi.org/10.3389/fmicb.2020.01342](https://doi.org/10.3389/fmicb.2020.01342). [hal-02991968](https:// HAL Id: )

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# Editorial: Microbial Ecotoxicology

Stéphane Pesce¹*, Jean-François Ghiglione², Edward Topp³ and Fabrice Martin-Laurent⁴

¹ INRAE, UR RiverLy, Villeurbanne, France, ² CNRS, UMR 7621 Laboratoire d'Océanographie Microbienne, Sorbonne Université, Observatoire Océanologique de Banyuls-sur-Mer, Banyuls-sur-Mer, France, ³ Agriculture and Agri-Food Canada, University of Western Ontario, London, ON, Canada, ⁴ AgroSup Dijon, INRAE, Univ. Bourgogne, Univ. Bourgogne Franche-Comté, Agroécologie, Dijon, France

**Keywords:** biodegradation, biodiversity, bioindicator, communities, ecosystem functions, pollutants, risk assessment

## Editorial on the Research Topic

### Microbial Ecotoxicology

In the age of the Anthropocene, the world is facing unprecedented environmental challenges that have multifactorial and interlinked causes including population growth, pollution, and climate change. The “One Health” and “EcoHealth” paradigms emphasize the urgent need to protect ecosystem health in order to ensure human well-being and food security (Naeem et al., 2016; Destoumieux-Garzón et al., 2018). It is noteworthy that the majority of the 17 United Nations Sustainable Development Goals (UN-SDGs) fundamentally link environmental health to human health and well-being (Blicharska et al., 2019).

Within this context, mitigating anthropogenic impacts on ecosystem functions and services is a paramount challenge. Perhaps because they are not visible, microorganisms that provide or support key ecosystem services have generally been neglected as endpoints of concern in environmental risk assessment frameworks (Brandt et al., 2015). This, in spite of the fact that microbial communities deliver ecological processes and ecosystem services that are essential to life on earth (Cavicchioli et al., 2019). Exposure to inorganic or organic chemical pollutants, sometimes at very low concentrations, has the potential to kill or inhibit sensitive environmental microorganisms, or disrupt their activities. As with all biology on earth, microorganisms are subject to multiple physical and chemical stressors, including mixtures of commercial chemicals, pharmaceuticals, pesticides, and other agents that reach the environment either by design or in waste streams. Setting acceptable standards for chemical pollution on the basis of microbial impacts remains a significant challenge (Rockström et al., 2009).

Over the last few decades, a wide range of studies has investigated the interactions between microorganisms and pollutants at different biological scales ranging from the molecular to community levels. These studies have contributed to the emergence and the development of a new Research Topic designated “microbial ecotoxicology” (Ghiglione et al., 2016), built on key concepts from both microbial ecology and “classical” ecotoxicology. This Research Topic has recently benefited from tremendous technological improvements in several related fields, including environmental chemistry, microbiology, and microbial ecology as well as molecular and so called “omics ecology” (Marco and Abram, 2019). Indeed, a wide range of tools are now available to characterize microbial responses at different biological levels following exposure to a large variety of pollutants and their transformation products. Those concern so-called “legacy pollutants” (e.g., metals and metalloids, pesticides, chlorinated solvents or polycyclic aromatic hydrocarbons, PAHs), but also pollutants of emerging concern (e.g., pharmaceuticals, nanoparticles, plastic debris, biopesticides, or cyanotoxins). These responses are very complex and include reciprocal interactions because of the capacity of microorganisms to modify the bioavailability of pollutants and to transform or degrade many of them. Microbially biodegradable pollutants include

**OPEN ACCESS**

Edited and reviewed by:
Eric Altermann,
AgResearch Ltd, New Zealand

*Correspondence:
Stéphane Pesce
stephane.pesce@inrae.fr

**Specialty section:**
This article was submitted to
Microbiotechnology,
a section of the journal
Frontiers in Microbiology

**Received:** 28 April 2020
**Accepted:** 26 May 2020
**Published:** 26 June 2020

**Citation:**
Pesce S, Ghiglione J-F, Topp E and Martin-Laurent F (2020) Editorial: Microbial Ecotoxicology. *Front. Microbiol.* 11:1342.
doi: 10.3389/fmicb.2020.01342
substances that were initially specifically designed to inhibit
microbial activities, such as some antibiotics (Cycon et al.,
2019). Therefore, and as nicely illustrated in the present
Research Topic bringing together 41 articles co-authored by
308 investigators, microbial ecotoxicology is a growing Research
Topic that overcomes disciplinary approaches and compartment
boundaries within ecosystems to assess the interactions between
both prokaryotic and eukaryotic microorganisms and a wide
range of pollutants with the final objective of tackling urgent
environmental and societal challenges.

MICROBIAL EVOLUTION AND
ADAPTATION TO POLLUTANTS:
RESULTING ENVIRONMENTAL BENEFITS
AND ASSOCIATED ECOLOGICAL COSTS

Mechanistic and evolutionary approaches are still needed to characterize and understand how microorganisms adapt to pollutants, not only to tolerate, resist or transform them, but also in some cases to take benefit from them as energy sources for metabolism and growth. Research in microbial ecotoxicology continuously contributes to identify and characterize undescribed mechanisms involved in detoxification and/or degradation of pollutants by different kinds of microorganisms. Bacterial membranes (Amin and Latif), surface layers (Chandramohan et al.), and external components such as extracellular polymeric substances constituting biofilm matrix (Mosharaf et al.) provide a barrier protecting microorganisms against diverse pollutants. This was nicely illustrated by Amin and Latif who coupled heteronuclear single-quantum coherence nuclear magnetic resonance (HSQC NMR) and scanning electron microscopy (SEM) to study and visualize the accumulation of mercury (Hg) on the cell surface of the Hg-resistant strain *Enterobacter* sp. AZ-15. Microbial detoxification systems involving pollutant sequestration are potentially useful to remove these substances from contaminated environments, such as wastewater (Mosharaf et al.). Extracellular enzymes can also be liberated in the surrounding environment to protect microorganisms through detoxification. Therefore, Karich et al. showed that two fungal unspecific peroxygenases from the basidiomycetous *Agrocybe aegerita* and *Marasmius rotula* were able to transform most of the compounds listed as priority pollutants by the United States Environmental Protection Agency (EPA). The fungal role in pollutant biodegradation was also highlighted by Carles et al. who described the comabolic degradation of the herbicide nicosulfuron by *Plectosphaerella cucumerina* AR1 isolated from *Alnus* leaf litter submerged in freshwater.

Evolution of microbial catabolic capabilities enhances the
self-purifying capacity of contaminated environments, an
important ecosystem service in both terrestrial and aquatic
systems. However, studying and understanding the mechanisms
that mediate biodegradation activity of recalcitrant pollutants
remains necessary to better estimate the efficiency of such
microbial processes and the resulting effects on pollutant fate and

persistence in the different environmental compartments. For
instance, Fanesi et al. demonstrated through the use of innovative
vibrational spectroscopy techniques that soil content in organic
matter and mineral particles is a strong driver of the metabolic
profile of a PAH-degrading bacterium, *Pseudomonas putida* G7.
Such knowledge is of particular interest to develop, improve, and
implement innovative and successful bioremediation strategies
for polluted soils and surface or ground waters (Donati et al.,
2019; Hermon et al.; Laroche et al.; Spini et al.). As an example,
a critical review of the role of marine microorganisms in
the biodegradation of plastic debris and on the relevance of
current standard tests for plastic biodegradability in seawater
ecosystems is provided in the present Research Topic (Jacquin
et al.). This review is complemented by an original study that
described the successive phases of colonization, growing, and
maturation phases of marine biofilms on non-biodegradable and
biodegradable plastics (Dussud et al.).

Besides potential environmental benefits due to the
development of biodegradation capacities, adaptation to
pollutants is, on a one hand, a key process that confers resistance
and resilience in exposed microbial communities supporting
the ecological functioning of contaminated ecosystems (Pesce
et al., 2017; Capdeville et al.). On the other hand, mechanisms
and processes driving microbial adaptation to pollutants at
individual level can represent a genetic burden decreasing the
fitness of adapted populations when the selection pressure by
the pollutant is released (Changey et al., 2011). Adaptive
responses to pollutants, including notably the acquisition of
tolerance, can be studied at the microbial community level. The
emergence, at the end of the twentieth century, of the concept
of pollution induced community tolerance (PICT; Blanck et al.,
1988), is one of the best illustrations of this kind of approach,
which is still currently used in microbial ecotoxicology to
assess the causal relationship between pollutant exposure and
microbial responses (e.g., Brandt et al., 2015; Tlili et al., 2016).
However, there is evidence that PICT is generally associated with
a decrease in diversity and the associated ecological functions
(Mahamoud Ahmed et al., 2020) in line with the paradigm
that biodiversity serves as ecological insurance (Yachi and
Loreau, 1999). These resulting costs of tolerance can be viewed
as ecological costs of adaptation (Clements and Rohr, 2009).
Indeed, loss of diversity in microbial communities following
pollutant exposure may not only alter the functions they support
but also increase their vulnerability to further environmental
disturbances. Conversely, environmental stressors (such as
warming; Lambert et al., 2017 or hydrodynamics; Polst et al.)
can influence microbial diversity and modify the capacity
of microbial communities to tolerate pollutant toxicity. The
development of pollutant-resistant species can also modify
community functional pattern and alter some metabolic
capacities (Cycon et al.). Moreover, within the One Health
framework, the development or acquisition of resistance to
antibiotics by environmental microorganisms is contributing
to the emergence of multi-drug-resistant human and animal
pathogens thus endangering livestock production and the
efficacy of medicines to treat infections (Smalla et al., 2016; Topp
et al., 2018).
POLLUTANT EFFECTS ON MICROBIAL
COMMUNITIES THREATEN ECOSYSTEM
BIODIVERSITY AND FUNCTIONS IN ALL
ENVIRONMENTAL COMPARTMENTS

Since the early 2000s, ecotoxicological studies (including “microbial ecotoxicology”) have progressively moved toward experimental designs that better assess and predict the ecological risks of a given chemical stressor under realistic environmental conditions. Several articles of this Research Topic highlight the potential effects of a wide range of pollutants on microbial structure, diversity and functions in contaminated soils (Borymski et al.; Cycon et al.; Mallet et al.; Simonin, Colman et al.; Simonin, Cantarel et al.), wastewaters (Guo et al.), continental (Chonova et al.; Freixa et al.; Pei et al.) and coastal surface water (Coclet et al.; Corcoll et al.; Zouch et al.), groundwater (Crampon et al.; Imfeld et al.), and sediments (Mahamoud Ahmed et al.). Such effects on microbial communities can threaten important ecosystem functions and services such as agricultural soil aggregation (Crouzet et al.), wastewater treatment (Guo et al.), primary production (Corcoll et al.), organic matter decomposition and nutrient cycling (Mahamoud Ahmed et al.; Rossi et al.; Simonin, Colman et al.), or energy transfer among trophic levels (Crenier et al.). Unsurprisingly, a large proportion of the above-mentioned studies concerns metal pollutants that are ubiquitously found in the environment due to the combination of natural and anthropogenic sources. Therefore, this Research Topic provides further evidence that metals are one of the major drivers of microbial community structure and diversity, affecting both bacteria, archaea and algae and the functions they ensure within ecosystems (Borymski et al.; Pei et al.; Coclet et al.; Corcoll et al.; Zouch et al.; Mahamoud Ahmed et al.). However, metals are also present in the environment as nanoparticles due to their high production and use for numerous applications. Simonin, Colman et al. and Simonin, Cantarel et al. showed that copper-based nanopesticides used as a fungicide and bactericide can impact microbial processes involved in soil carbon and phosphorus cycling after chronic exposure, revealing that short-term studies may underestimate the ecotoxicological risks of these new generation of metallic pesticides on soil microbial communities and ecosystem functioning. Other metal nanoparticles, such as zero-valent iron nanoparticles that are used for remediation of different kinds of pollutants (Crampon et al.) or silver nanoparticles that are used for antimicrobial treatment (Guo et al.), were also shown to present risks for bacterial community structure and metabolic potential. As nanopesticides, biobased pesticides are often viewed as a safe alternative to synthetic organic pesticides in agriculture to achieve the agroecology transition (Seiber et al., 2014). However, ecotoxicological risks and effects of these natural active substances are still under documented (Amichot et al., 2018). The study of Mallet et al. provides evidence that natural β-triketone herbicide leptospermone can impact the composition and diversity of fungal communities in arable soils. All these results underline the need of incorporating microbial endpoints for environmental risk assessment and homologation processes

of novel agrochemicals such as nanopesticides or biobased
pesticides. Those are viewed as pollutants of emerging concerns,
such as pharmaceuticals or plastics, which are also taken into
consideration in this Research Topic (Chonova et al.; Cycon
et al.; Dussud et al.; Freixa et al.; Jacquin et al.; Orlewska
et al.). Cyanotoxins are also sometimes cited as pollutants of
emerging concerns (Snow et al., 2017) that can be harmful to
both environmental and human health. Using a metabolomics
approach, Le Manach et al. reported the production of a
wide set of metabolites by 24 *Microcystis* strains, including
different classes of cyanotoxins together with a large set of
unknown molecules.

However, assessing and predicting the consequences of legacy
pollutants or pollutants of emerging concerns on ecosystem
functions and services remains a challenge because multiple
stressors proceed simultaneously on complex interconnected
biological communities. For a better understanding of the
chain of causality starting from pollutant exposure to microbial
community responses and then mediated ecosystem alteration,
microbial ecotoxicological approaches and indicators that
take into account the possible interactions between multiple
pollutants are needed (Freixa et al.; Mahamoud Ahmed et al.).
Therefore, Freixa et al. showed that carbon nanoparticles
(fullerenes C60) can modulate the effects of organic pollutants on
aquatic biofilm communities. However, they observed that both
the magnitude and the direction of the interaction following joint
exposure varied regarding the kind of organic pollutant, being
sometimes antagonistic (e.g., fullerenes C60/diuron), synergistic
(fullerenes C60/triclosan), or neutral (fullerenes C60/venlafaxine)
(Freixa et al.). Effect interactions can also vary according to
the microbial endpoint considered. For instance, Mahamoud
Ahmed et al. observed that arsenic and copper had an additive or
synergetic negative impact on sediment denitrification while no
interaction was recorded when considering other functions such
as respiration or several extracellular enzymatic activities.

Moreover, interactions between pollutants and other
environmental abiotic and biotic stressors must also be
considered since they can modulate both the exposure and
the sensitivity of microbial communities to toxicants. These
parameters can be both physical, such as temperature (Pesce
et al.) or hydrodynamic (Polst et al.), chemical, such as nutrients
(Crenier et al.; Rossi et al.; Simonin, Cantarel et al.) or salinity
(Rotini et al.), or biological (Bart et al.). More frequent studies
evaluating the impact of combined or cumulative exposure to
multiple chemical and non-chemical stressors on microbial
communities in controlled conditions or along environmental
gradients are being published (see above examples). Nevertheless,
it is still difficult to go beyond these case-by-case studies and to
generalize concepts that can be deployed widely in environmental
risk assessment procedures. Large-scale initiatives (i.e., meta-
studies) such as the “Microbiome Stress Project” proposed by
Rocca et al. to leverage existing metagenomic studies assessing
the response of microbial communities to various environmental
stressors are timely. The crucial issue of data-sharing has recently
been pinpointed by Eckert et al. (2020) who claimed that at least
20% of published metagenomic data are not generally accessible
for other scientists, and lack robust metadata.
RESEARCH IN MICROBIAL
ECOTOXICOLOGY SHOULD IMPROVE
POLLUTANT RISK ASSESSMENT AND
ECOSYSTEM QUALITY MONITORING BUT
LACKS ROBUST TRANSFER TO
STAKEHOLDERS AND ENVIRONMENTAL
MANAGERS

Microbial ecotoxicology is a growing Research Topic that
contributes to improve knowledge on the microbial responses
to pollutants under variable exposure scenarios. Furthermore,
innovative methods and approaches are being developed
including novel ecotoxicological endpoints (Sgier et al.), new
types of bioassays (Morin et al.) and next generation methods,
such as volatolomics to detect signatures of pollutant exposure
(Hidalgo et al.). Efforts have also been made to develop
and test bioindicator approaches to assess biological exposure
to pollutants and/or resulting effects on ecological quality
in contaminated ecosystems through the study of microbial
communities naturally present in the different environmental
compartments (Imfeld et al.; Pei et al.; Pesce et al., 2017).
However, despite strong evidence of the relevance of developed
methods and approaches, these remain case studies that do
not entirely respond to the needs of environmental regulators
and managers. Operational and generalizable procedures have
not been examined so far, from sampling strategies to data
analysis, including tests for robust interpretation methodologies
with reference baselines and quality levels. Accordingly, changes
in microbial assemblages are still not well taken into account
for pollutant risk assessment and ecosystem quality monitoring,
as regularly pointed out, for example, by the European
Food Safety Authority (EFSA PPR Panel, 2013, 2017; EFSA
Scientific Committee, 2016). As an example, potential impacts
on microbial communities are completely ignored in the
development of Environmental Quality Standards (EQS) in
the EU water framework directive (WFD) that is the most
significant European water legislation to date. These EQS
mandate concentration thresholds that should not be exceeded
for a range of selected pollutants to preserve ecological
integrity in aquatic ecosystems. Only diatom biodiversity is
used to assess the biological quality of water bodies within
the WFD.

In 2016, Bengtsson-Palme and Larsson (2016) also
underlined the need for considering the risks of antibiotic
resistance development associated with antibiotic pollution
and subsequent dissemination to human pathogens. They
determined “predicted no effect concentrations” (PNECs)
for 11 selected antibiotics based on available minimum
inhibitory concentrations (MICs). Most of the PNECs were
below available PNECs for ecotoxicological effects, suggesting
that current environmental guidelines are not protective
enough for environmental and human health (Tell et al.,
2019).

KEY CHALLENGES AND FUTURE
PERSPECTIVES

Knowledge about the interactions between pollutants and microbial communities is continuously increasing. The following challenges, which are far from being exhaustive, underline the necessity (i) to reinforce disciplinary knowledge to better characterize microbial responses to pollutants at the species, population, and community levels but also (ii) to develop multi-disciplinary approaches combining among others microbial ecotoxicology, ecology, microbiology, toxicology, environmental chemistry and physics, big data science, modeling, as well as animal and human health sciences to better explore and predict the consequences of these responses on ecosystem and human health and well-being, in line with the “One Health” paradigm.

A major challenge is to go beyond the community level, which
is commonly considered in microbial ecotoxicology (Ghiglione
et al., 2016) in order to translate the microbial response to
ecosystem scale. This is the policy-relevant scale to which
prevention and mitigation strategies need to be deployed. This
crucial and non-trivial issue goes beyond the sole scope of
microbial ecotoxicology and needs the inclusion of the latest
advances and concepts in microbial ecology (Graham et al., 2016)
but also in general ecology to take into account the interactions
between micro- and macro-organisms. The short- and long-
term ecological costs of microbial adaptation processes (at both
the species and community levels), as well as community and
ecosystem resistance and resilience capacities that guarantee the
preservation and/or the recovery of ecosystem biodiversity and
functioning under pollutant exposure, need to be characterized.
This cannot be done without taking into account the fact that
microbial communities are generally chronically exposed to
complex mixtures of pollutants and are otherwise subjected to
a wide range of additional chemical, physical, and/or biological
stressors. This is conceptually and technically challenging since
the enormous diversity of pollutants and possible environmental
stressors preclude the testing of every possible binary and
multiple combinations. To face this gap, initiatives aiming to
facilitate data sharing from multistress studies and their meta-
analysis are greatly encouraged. Together with studies developing
mechanistic models of interaction at different levels, these
initiatives will be needed to produce robust and generalizable
predictive models for the purposes of improving the a priori
and a posteriori risk assessment of pollutants in the context of
global change.

Another main challenge concerns the urgent need of
extending our knowledge on the environmental factors
(including pollutants) and the microbial mechanisms that
contribute to the development, the proliferation and the
dispersal of pathogenic microorganisms, microbial resistance to
pharmaceuticals and microbial toxins in various environmental
compartments. Managing microorganisms of human or animal
health concern requires consideration of the environmental
dimension of the One Health Continuum.
Finally, future research in microbial ecotoxicology should also gain in transferability to end-users, including policy-makers and environmental managers, to develop more effective policies and efficient regulations aiming at preserving our environment and health from the adverse effects of pollutants. We mentioned above the need of better considering microbial communities, their functional diversity and their role in the evolution and spreading of antibiotic-resistant pathogens in the elaboration of Environmental Quality Standards (EQS) and in homologation procedures (including those of nanopesticides or biobased pesticides). Given how rapidly research in microbial ecotoxicology and related methods are developing, it is a challenge to identify, standardize, and normalize the most relevant protocols for operational and regulatory applications. Indeed, standards are required (Philippot et al., 2012; Römbke et al., 2018) and large-scale studies are needed to perform meta-analyses and inform models to establish reference baselines, such as “normal operating ranges” of microbial functions (EFSA Scientific Committee, 2016). Moreover, one may not exclude the fact that the microbial world, which is most often invisible to the human eye, remains largely unknown to the general public and, even more worryingly, to a wide range of stakeholders and deciders. Among others, this is probably one of the main

reasons why knowledge transfer from science to end-users and other stakeholders is particularly poor and has to be improved. It is thus important to have a dialogue between the research community, regulators, industry and broader society in order to share a common understanding making possible the achievement of a societal consensus defining the acceptable effect of pollutants on microbial communities and supported ecosystem services.

## AUTHOR CONTRIBUTIONS

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

## ACKNOWLEDGMENTS

This Research Topic was promoted by the International Network on Microbial Ecotoxicology - EcotoxicoMic (https://ecotoxicomic.org/). We thank all participating authors and reviewers for having made this Research Topic a success. We are also grateful to Dr. Philippe Garrigues for his support and help since the early stages of development of the EcotoxicoMic Network.

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**Conflict of Interest:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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