Low temperature reduces byssus adhesion of highly invasive golden mussels: Influencing mechanisms and antifouling implications

Byssus adhesion-based biofouling by invasive mussels poses threats to freshwater ecosystems and underwater facilities worldwide. Among existing antifouling strategies, high-temperature treatment is commonly used to eliminate biofouling by killing mussels or reducing byssus adhesion. However, despite its effectiveness, this method is limited by high energy consumption and the potential for damage to facility surfaces. Low-temperature treatment offers a promising alternative for freshwater antifouling; however, its underlying mechanisms remain poorly understood. Here, we used the invasive golden mussel (Limnoperna fortunei) as a model species to investigate the mechanisms by which low temperatures (15 °C and 5 °C) affect byssus adhesion and biofouling. Our results showed that low-temperature exposures significantly reduced adhesion rates of golden mussels, primarily by limiting byssus production associated with impaired synthesis and secretion of byssal proteins and decreasing byssus breaking force. Staining analysis observed foot gland atrophy and thickened collagen, suggesting disrupted byssal protein secretion. Additionally, reduced levels of tyrosinase and polyphenol oxidase further suggested the decreased byssus structural integrity due to disrupted byssal protein cross-linking. Both individual and integrated transcriptomic and metabolomic analyses confirmed the down-regulations of genes and pathways associated with byssal protein synthesis (e.g., mussel foot proteins and aromatic amino acid biosynthesis pathway) and up-regulations of metabolites related to protein cross-linking disruption. These changes collectively restricted byssal protein synthesis, protein precursor availability, and protein cross-linking processes. Notably, integrated transcriptomic and metabolomic analyses also revealed that low-temperature exposures activated survival-prioritized responses, including antioxidant, cellular stress response, immune regulation, and anti-apoptosis. The activation of energy-intensive defenses triggered an energy trade-off, reallocating energy from byssus production to stress responses and contributing to the reduced byssus adhesion of golden mussels under low temperatures. Collectively, our results reveal that low temperatures reduce golden mussel byssus adhesion by disrupting byssal protein synthesis, secretion, and cross-linking through integrated morphological, molecular, and metabolic pathways. The findings in this study advance our understanding of low-temperature treatment as a potential strategy for controlling freshwater mussel biofouling and provides a crucial foundation for developing targeted, environmentally sustainable antifouling approaches in aquatic ecosystems.This dataset contains comprehensive transcriptomic and metabolomic data investigating the molecular mechanisms underlying the impact of low-temperature stress on byssal adhesion in mussels. It integrates results from differential expression analyses, pathway enrichment, and co-expression networks. Included are the differentially expressed genes (DEGs) and metabolites (DEMs) used for generating heatmaps and identified as shared across four experimental comparison groups via Venn diagrams. Results from Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analyses for both transcriptomic and metabolomic data across all comparison groups are provided. The dataset further encompasses outputs from co-expression network analyses, detailing the identified DEGs and DEMs within key modules, along with specifically selected DEMs from these networks. Finally, it includes integrated DEG and DEM data from co-enrichment pathway analyses, revealing coordinated biological pathways significantly altered under low-temperature conditions. Collectively, these nine interconnected tables provide a foundational resource for understanding the molecular and metabolic adaptations (or disruptions) associated with impaired byssal thread production and adhesion during low-temperature exposure, facilitating future comparative studies in molluscan physiology, bioadhesion, and environmental stress responses.