Kaede Miyata

Mutagenicity and genotoxicity research has traditionally focused on evaluating how chemicals affect genomes, particularly in relation to mutation-driven carcinogenesis. Advances in next-generation sequencing have broadened environmental applications, enabling eDNA/eRNA analysis, metagenomics, and wastewater-based surveillance for ecosystems and public health monitoring. Framed within a One Health perspective that links human, animal, and environmental health, this Global Perspective examines synergies between mutagenomics and environmental genomics aimed at maintaining organismal and ecosystem health. We review emerging trends across five domains including antimicrobial resistance genes, pathogen dynamics, biodiversity, environmental stress responses, and biological evolution and discuss how integrating mutation genomics and molecular toxicology techniques into environmental monitoring can address current gaps. Common challenges include sensitive detection of low-frequency variants in mixed environmental samples, functional interpretation and causal attribution of variants and expression changes, and the lack of cross-taxonomic reference resources. Overcoming these challenges with mutation-genomics-derived approaches could enable improved source attribution, earlier detection of emerging threats, and outcome-oriented risk assessment. Now is the time to strengthen interdisciplinary collaboration, standardize methods, and establish cross-taxonomic reference and analytical infrastructures.

The symposium “New Approaches to Assessing the Environmental Impact of Chemicals: Bridging Ecotoxicology and Ecology through Environmental DNA/RNA Monitoring” was held on December 2, 2024 during the 7th annual meeting of The eDNA Society in Tsukuba, Japan. With increasing concerns about biodiversity loss and chemical pollution, the symposium aimed to explore innovative methodologies that assess ecological impacts from both chemical and biodiversity perspectives. Presentations addressed various applications of environmental DNA (eDNA) and RNA (eRNA) technologies, including ecological effect assessments of pesticides and metals as well as noninvasive biological stress profiling. This report summarizes the key discussions and insights from the symposium, highlighting the potential of eDNA and eRNA in integrating ecotoxicology with ecological assessments to achieve “Nature Positive” outcomes.

To achieve the current Nature Positive goals, it is important to identify the effects of chemicals on ecosystems and strategically reduce their risks. We therefore estimated the safe concentration (SC) of linear alkylbenzene sulfonate (LAS) by investigating the relationship between benthic communities detected via environmental RNA (eRNA) and environmental DNA (eDNA) metabarcoding and the water quality in a river contaminated with LAS. Non-metric multidimensional scaling of benthic communities detected via eRNA indicated significant differences between contaminated and non-contaminated sites, and redundancy analysis showed significant correlation between the benthic communities and LAS concentration. These results demonstrate that eRNA is more sensitive than eDNA for capturing the community changes that result from LAS contamination. No significant differences were observed in biodiversity indices between the highest LAS concentration site and non-contaminated site; thus, the SC was estimated at >47 µg/L. The results suggest that, although hazard assessment using the assessment factor (AF) leads to conservative estimation of the effects of chemicals because the predicted no-effect concentration in previous studies is lower than the SC, hazard assessment based on the response of biological communities using eRNA metabarcoding can refine such ecological assessments, developing the environmental management standards to achieve nature-positive goals.

Metabarcoding analysis using fish environmental RNA (eRNA) has demonstrated higher performance compared to that using fish environmental DNA (eDNA) in the Naka River in Japan. However, the results from representative sampling sites were insufficient to estimate the diversity of organisms in the entire river. Therefore, we validated the evaluation performance using additional traditional field survey (TFS) data. Data from seven traditional field surveys on fish, covering the area near the sampling points where eDNA/eRNA metabarcoding analyses were conducted, were obtained. Ten fish species were newly identified, with nine determined using the eDNA and eRNA metabarcoding analyses. Performance was evaluated in terms of both positive predictive value (PPV) and sensitivity. Except for species specifically detected only near the estuary, the additional use of field survey data increased the PPV from 26.5% to 36.3% for eDNA and from 43.6% to 57.7% for eRNA. After combining the results of multiple surveys, the sensitivities for eDNA and eRNA increased from 52.4% to 67.4% and from 57.1% to 69.8%, respectively. The increase in PPV was more pronounced for eRNA than for eDNA, indicating that eRNA does not decrease PPV when multiple datasets are merged. The superior performance of eRNA compared to eDNA suggests that eRNA metabarcoding analysis is valuable for accurately conducting ecological surveys and biodiversity assessments and may reduce the labor required for monitoring the entire river by optimizing sampling points for metabarcoding analysis.

The symposium “The New Era Shaped by Environmental Genome Monitoring,” held in December 2024 by the Japanese Environmental Mutagen and Genome Society (JEMS), aimed to explore the interdisciplinary collaborations that are essential for the development of new scopes in environmental genome monitoring. This event highlighted the necessity of integrating mutagenicity research with ecological assessments to enhance public health and biodiversity conservation. Presentations focused on the evolving landscape of environmental genomics, including metagenomic analyses for antibiotic resistance, viral genomic surveillance in wastewater, and innovations in noninvasive biodiversity and stress monitoring through environmental DNA and RNA. This report summarizes the key discussions and presentations from the symposium, underscoring the critical role of environmental genome monitoring in shaping future safety research.

The utility of environmental RNA (eRNA) in capturing biological responses to stresses has been discussed previously; however, the limited number of genes detected remains a significant hindrance to its widespread implementation. Here, we investigated the potential of eRNA to assess the health status of Japanese medaka fish exposed to linear alkylbenzene sulfonate. Analyzing eRNA and organismal RNA (oRNA) in aquarium water for > 12 h, we achieved high mapping rates and 10 times more differentially expressed genes than previously reported. This advancement has facilitated the previously unattainable capability of gene ontology (GO) analysis. In GO analysis, it was found that eRNA could detect nuclear genes in cellular component, and oRNA provided gene expression signatures in the short term, whereas eRNA demonstrated the potential to reflect cumulative gene expression signatures over a period of time in biological process. Moreover, eRNA exhibited high sensitivity in responding to genes associated with sphingolipid and ceramide biosynthesis, which are involved in inflammatory responses possibly originating from impaired cells. This finding aligns with the observations made in oRNA. Conclusively, eRNA-sequencing (eRNA-seq) using aquarium water emerges as a valuable high sensitivity tool for analyzing physiological stress. The findings of this study lay the foundation for further development of eRNA-seq technologies.

Coral reefs are at risk of bleaching due to various environmental and anthropogenic stressors such as global warming and chemical pollutants. However, there is little understanding of stressor-specific mechanisms that cause coral bleaching. Therefore, conducting accurate ecotoxicological risk assessments and deciphering modes of action of potentially deleterious ultraviolet (UV) filters (sunscreen compounds) are crucial issues. In this study, we evaluated the toxicity and bleaching effect of benzophenone-3 (BP-3), which is widely used in sunscreen products, on the reef-building coral Acropora tenuis . Furthermore, to understand differences in UV filter- and temperature-induced bleaching, a comparative ecotoxicogenomic approach using RNA-seq was integrated into a toxicity test to clarify differences in gene expression changes induced by BP-3 and heat stress (31°C). The lethal concentration 50% (LC50) was calculated as 3.9 mg/L, indicating that emission level of BP-3 was properly controlled based on the risk assessment. Differentially expressed genes related to oxidative stress and extracellular matrix organization were involved in coral responses to both BP-3 and heat stress, but their patterns differed. Whereas immune and heat-shock responses were activated in response to heat stress, activation of a drug metabolism pathway and several signal transduction pathways were identified in BP-3 treatment groups. Our study enhances understanding of stress responses in corals induced by UV filters and thermal stress. Using potential gene markers identified in this study for eco-epidemiological surveys of stressed corals, we urgently need to develop effective countermeasures.