Ecosystems monitoring powered by environmental genomics: A review of current strategies with an implementation roadmap

Abstract

A decade after environmental scientists integrated high-throughput sequencing technologies in their toolbox, the genomics-based monitoring of anthropogenic impacts on the biodiversity and functioning of ecosystems is yet to be implemented by regulatory frameworks. Despite the broadly acknowledged potential of environmental genomics to this end, technical limitations and conceptual issues still stand in the way of its broad application by end-users. In addition, the multiplicity of potential implementation strategies may contribute to a perception that the routine application of this methodology is premature or "in development", hence restraining regulators from binding these tools into legal frameworks. Here, we review recent implementations of environmental genomics-based methods, applied to the biomonitoring of ecosystems. By taking a general overview, without narrowing our perspective to particular habitats or groups of organisms, this paper aims to compare, review and discuss the strengths and limitations of four general implementation strategies of environmental genomics for monitoring: (a) Taxonomy-based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics). We emphasise the utility of the three latter strategies to integrate meiofauna and microorganisms that are not traditionally utilised in biomonitoring because of difficult taxonomic identification. Finally, we propose a roadmap for the implementation of environmental genomics into routine monitoring programmes that leverage recent analytical advancements, while pointing out current limitations and future research needs.

Keywords: biodiversity; biomonitoring; ecosystem management; environmental DNA; implementation strategy; metabarcoding.

FIGURE 1

Overview of the current methodology for the monitoring of ecosystems, that relies mostly on the morphological identification of biodiversity and/or bioindicators of anthropogenic impacts. Ecological diagnostics are performed based on reference biodiversity or on reference biotic indices for a given ecosystem. The development of environmental genomics methodologies has led to the proposition of multiple implementation strategies that can intervene at different levels of the monitoring workflow, to produce an ecological diagnostic. Green colours and smileys within boxes indicate reference biodiversity and "good" or “high” ecological status while red colours and smileys represent nonreference biodiversity and “poor” ecological status (i.e., impacted environments) Green colours and smileys within boxes indicate reference biodiversity and "good" or “high” ecological status while red colours and smileys represent nonreference biodiversity and “poor” ecological status (i.e., impacted environments). The colours on tags besides organisms or sequences indicate their bioindication value (red: indicator of impact, yellow: indicator of intermediate status, green: indicator of good status). In this review paper, these strategies have been grouped into four broad categories: (a) Taxonomy‐based analyses focused on identification of known bioindicators or described taxa; (b) De novo bioindicator analyses; (c) Structural community metrics including inferred ecological networks; and (d) Functional community metrics (metagenomics or metatranscriptomics)

FIGURE 2

Strengths and limitations of the currently envisioned implementation strategies of environmental genomics for the monitoring of ecosystems, and their ability to fulfill the criteria of existing monitoring programmes. The tag above organisms indicate their taxonomic affiliation and smileys indicate the ecological status of the sample (from "poor" to "good")