Coping with extremes: How Epigenetic and Molecular Adaptations Enable Earthworms to Thrive in Volcanic Soils

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Abstract Earthworms thriving in naturally occurring geothermal soils offer rare insight into rapid adaptation to environmental extremes. Here, we show that the pantropical earthworm Amynthas gracilis survives and flourishes in soils of the Furnas Volcano (São Miguel Island, Azores), where conditions include elevated temperatures (up to 40 °C), high CO 2 (88.6%), low O 2 (10%), toxic metals, and mildly acidic pH. In a reciprocal-transplant, mesocosm-based experiment between soils overlying areas of active degassing volcanic gassing (hereafter active degassing soils) and reference soils, convergence of the epidermal thickness of the transplanted earthworms to the resident-soil phenotype (24 ± 3.9 µm active degassing soil, 43.8 ± 8 µm reference soil), was observed within 31 days. Combining RNA-Seq, DNA (5-cytosine) methylation mapping, and microRNA profiling, this phenotypic change results from coordinated transcriptional and epigenetic reprogramming. While gene-body methylation occurred at ∼98 % of loci, levels varied, and differentially methylated regions were enriched ffor genes with altered expression under volcanic stress. Multi-omics network analysis identified epithelial morphogenesis, circulatory system formation, and neural development as regulatory hubs, highlighted by a set of 41 epithelial-morphogenesis genes showing consistent methylation and miRNA patterns. Additional modules governing ion transport and signal transduction complemented the adaptive response. Collectively these findings demonstrate that A. gracilis employs dynamic DNA methylation and microRNA regulation alongside transcriptional reprogramming to generate a persistent phenotypic adjustment to a volcanic stress. This work advances our understanding of extremophile resilience and provides a scalable model for predicting organismal adaptive capacity in the face of environmental extremes.

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