Microbiome-Aware Ecotoxicology of Organisms: Relevance, Pitfalls, and Challenges

Abstract

Over the last 15 years, the advent of high-throughput "omics" techniques has revealed the multiple roles and interactions occurring among hosts, their microbial partners and their environment. This microbiome revolution has radically changed our views of biology, evolution, and individuality. Sitting at the interface between a host and its environment, the microbiome is a relevant yet understudied compartment for ecotoxicology research. Various recent works confirm that the microbiome reacts to and interacts with contaminants, with consequences for hosts and ecosystems. In this paper, we thus advocate for the development of a "microbiome-aware ecotoxicology" of organisms. We emphasize its relevance and discuss important conceptual and technical pitfalls associated with study design and interpretation. We identify topics such as functionality, quantification, temporality, resilience, interactions, and prediction as major challenges and promising venues for microbiome research applied to ecotoxicology.

Keywords: contaminants; environment; microbiota; resilience; symbiosis; toxicology.

Figure 1

Ecotoxicology studies the effect of chemicals on organisms at the population level. A microbiome-aware ecotoxicology perspective acknowledges the importance of associated microorganisms in their hosts biology, at the level of individuals as well as populations. Indeed, the microbiome is interacting with hosts, environment, and contaminants and may be linked with health status (here, light vs. dark gray). The microbiome thus needs to be integrated as an element of the system, and protocols to investigate ecotoxicological effects at each level need to be adapted.

Figure 2

Sitting at the interface between environment and host, the microbiome may interact with contaminants. Sequestration, inactivation, and degradation mitigate potential effects on host health, while activation or potentialization reinforce the effect of contaminants. Microbiome composition, abundance and functions respond to exposure, and dysbiosis can occur. Post-exposure recovery leads to a new stable state, identical, or altered compared to the pre-exposure state. Future lines of research are emphasized. Although contaminants may alter the host health through adverse outcome pathways, dysbiosis itself may also induce pathology and fitness loss, difficult to disentangle from each other.