Environmental hypoxia, increasingly prevalent due to climate change and eutrophication in southern Chilean fjords, represents a critical threat to the sustainability of Mytilus chilensis aquaculture. This study investigated the integrated transcriptomic and microbiota responses of M. chilensis to prolonged hypoxia (2 mg L⁻¹) for 10 days and subsequent reoxygenation for 10 days over a 60-day period, compared to normoxic controls (7.2 ± 0.2 mg L⁻¹). A total of 480 adult mussels were utilized to assess tissue-specific transcriptomic changes via RNA-seq in gill, digestive gland, and adductor muscle, and to characterize microbiota dynamics in gill and digestive gland using 16S rRNA nanopore sequencing.
Transcriptomic profiling revealed significant differential expression across tissues, with 15,056, 11,864, and 9,862 transcripts modulated in gill, digestive gland, and muscle, respectively. Chromosomal clustering of differentially expressed genes was observed on Chr1, Chr9, and Chr10. Gene Ontology (GO) enrichment analyses highlighted the upregulation of pathways related to endoplasmic reticulum stress, TORC1 signaling, and apoptosis under hypoxic conditions. Concurrently, downregulation of immune signaling pathways, including Toll-like and NF-κB, suggests hypoxia-induced immunosuppression and a shift towards anaerobic metabolic adaptation. Specifically, genes associated with ER stress response and apoptosis were significantly upregulated in gills, indicating cellular damage and programmed cell death.
Microbiota analysis demonstrated hypoxia-driven dysbiosis, characterized by a reduction in alpha diversity and a significant increase in the relative abundance of facultative anaerobic bacteria, notably Vibrio and Aeromonas. This shift was accompanied by a decrease in the abundance of beneficial taxa, such as Rhodobacterales. Functional annotation of the altered microbial communities indicated a decline in pathways associated with nutrient metabolism and immune modulation, mirroring the observed host transcriptomic suppression. For example, Vibrio species showed a significant increase in hypoxia, suggesting their adaptation to low oxygen conditions and potential opportunistic behavior.
These findings provide compelling evidence that hypoxia induces a complex, dual-layered stress response in M. chilensis, involving both significant host genomic reprogramming and substantial restructuring of the associated microbial community. The integrated omics approach employed in this study offers valuable insights and potential biomarkers for the development of climate-adaptive aquaculture strategies and improved resilience forecasting in the face of increasing environmental stressors.