Exposure to complex mixtures of urban sediments containing Tyre and Road Wear Particles (TRWPs) increases the germ-line mutation rate in Chironomus riparius

Aquatic Toxicology, vol. 281, pp. 107292

Abstract

Tyre and road wear particles (TRWPs) are a significant yet often underestimated source of environmental pollution, contributing to the accumulation of microplastics and a complex mixture of contaminants in both terrestrial and aquatic ecosystems. Despite their prevalence, the long-term evolutionary effects of TRWPs, beyond their immediate toxicity, remain largely unknown. In this study, we assessed mutagenicity in the non-biting midge Chironomus riparius, upon exposure to urban sediment collected from a runoff sedimentation basin. To assess the extent of mutagenic effects over multiple generations, we combined the urban sediment exposure model with short-term mutation accumulation lines (MALs) and subsequent whole genome sequencing (WGS). The study was conducted over five generations, with urban sediment concentrations of 0.5 % and 10 %. Our results reveal that the exposure to urban sediment significantly increases mutation rates compared to control groups by 50 %, independent of concentration (0.5 % and 10 %). To infer potential causal processes, we conducted a comparative analysis using known mutational spectra from previous studies. This comparison showed that the mutation profiles induced by urban sediment clearly clustered with those caused by Benzo[a]Pyrene (BaP), a known Polycyclic Aromatic Hydrocarbon (PAH). A comprehensive chemical characterization of the sediment confirmed a considerable impact of road runoff and traffic-related contamination, including PAHs of primarily petrogenic origin. This suggests that PAH-like compounds present in urban sediments may play a significant role in the observed mutagenic effects. Our study shows that urban sediments influence mutation rates and alter mutational spectra in exposed organisms, potentially compromising genomic stability and shaping evolutionary trajectories. These genetic changes can have profound long-term effects on population dynamics and ecosystem health, underlining the importance of understanding the evolutionary consequences of environmental pollution. Additionally, we show that comparatively analysing of mutational spectra may provide valuable insights into mutational processes.

Authors 5

1. Markus Schmitz

   Goethe University Frankfurt

   Affiliation as printed

   Department of Evolutionary Ecology & Environmental Toxicology (E3T), Institute for Ecology, Evolution and Diversity, Faculty 15 Biological Sciences, Goethe University Frankfurt am Main, Germany

2. Volker Linnemann Aachen Institute for Environmental Engineering

   RWTH Aachen University

   Affiliation as printed

   Institute for Environmental Engineering, RWTH Aachen University, Germany

3. Martin Krayer Von Krauss

   Helmholtz Centre for Environmental Research

   Affiliation as printed

   Department of Exposure Science, Helmholtz Centre for Environmental Research - UFZ, 04318 Leipzig, Germany

4. Henner Hollert

   Goethe University Frankfurt · LOEWE Centre for Translational Biodiversity Genomics · Fraunhofer Institute for Molecular Biology and Applied Ecology · Senckenberg Biodiversity and Climate Research Centre

   Affiliation as printed

   LOEWE Centre of Translational Biodiversity Genomics, Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, D-60325, Frankfurt am Main, Germany; Department of Evolutionary Ecology & Environmental Toxicology (E3T), Institute for Ecology, Evolution and Diversity, Faculty 15 Biological Sciences, Goethe University Frankfurt am Main, Germany; Department Environmental Media Related Ecotoxicology, Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Schmallenberg, Germany

5. Markus Pfenninger

   Johannes Gutenberg University Mainz · LOEWE Centre for Translational Biodiversity Genomics · Senckenberg Biodiversity and Climate Research Centre

   Affiliation as printed

   Department of Molecular Ecology, Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, D-60325, Frankfurt am Main, Germany; LOEWE Centre of Translational Biodiversity Genomics, Senckenberg Biodiversity and Climate Research Centre, Georg-Voigt-Str. 14-16, D-60325, Frankfurt am Main, Germany; Institute for Molecular and Organismic Evolution, Johannes Gutenberg University, Johann-Joachim-Becker-Weg 7, D-55128, Mainz, Germany