Unlocking secrets of microbial ecotoxicology: recent achievements and future challenges

Abstract

Environmental pollution is one of the main challenges faced by humanity. By their ubiquity and vast range of metabolic capabilities, microorganisms are affected by pollution with consequences on their host organisms and on the functioning of their environment. They also play key roles in the fate of pollutants through the degradation, transformation, and transfer of organic or inorganic compounds. Thus, they are crucial for the development of nature-based solutions to reduce pollution and of bio-based solutions for environmental risk assessment of chemicals. At the intersection between microbial ecology, toxicology, and biogeochemistry, microbial ecotoxicology is a fast-expanding research area aiming to decipher the interactions between pollutants and microorganisms. This perspective paper gives an overview of the main research challenges identified by the Ecotoxicomic network within the emerging One Health framework and in the light of ongoing interest in biological approaches to environmental remediation and of the current state of the art in microbial ecology. We highlight prevailing knowledge gaps and pitfalls in exploring complex interactions among microorganisms and their environment in the context of chemical pollution and pinpoint areas of research where future efforts are needed.

Keywords: diversity; ecosystem functions; holobiont; microorganisms; nature-based solutions; pollution.

Figure 1.

The multiple scales of microbial ecotoxicology, at molecular, cellular, community (including interactions), and ecosystem levels.

Figure 2.

Possible outcomes in microbial community responses to pollutant disturbance with respect to a function of interest. (A) Model community initially composed of seven equally abundant taxa, some of which are capable of performing the function of interest (green star). This function may be directly associated with pollutant transformation, with another specific function (e.g. nitrogen fixation or nitrification), or with a widely distributed function (e.g. oxygen respiration). (B) Selected response profiles of microbial communities to disturbance (lightning) in terms of the function of interest (solid green line, left y-axis) and of taxonomic diversity (dashed black line, right y-axis). (C) Examples of microbial communities compatible with the different response profiles shown in (B) following pollution disturbance of the model community shown in (A). Apparent functional resistance to chemical pollution may involve loss of taxonomic diversity or functional redundancy, which will be detrimental for ecosystem functioning in the long-term. Functional resilience, i.e. the recovery of a particular microbially determined function following pollution disturbance, may feature changes in the taxonomic profile of the microbial community acting on the pollutant and gain of the functional ability to transform or degrade the pollutant by a resistant taxon through horizontal gene transfer, as shown. Of course, other community responses are also possible, such as gain of a degradation function upon pollution disturbance without apparent change of taxonomic diversity.

Figure 3.

Overview of the current gaps and limitations of the main methods for studying microorganisms (diversity, activities) at different levels of complexity and perspectives for data interpretation and diagnostic tool development.

Figure 4.

An overview of microbial transformation and degradation mechanisms of metals and metalloids (left) and organic molecules (right).

Figure 5.

Illustration of the current paradigm shift and how impacts of pollutants on microbial community diversity and functions can in turn affect host and ecosystem functioning.

Figure 6.

Illustration of different applications of microorganisms as tools for ERA and bioremediation.