Novel insights into deep-sea hydrothermal vent and cold seep adaptation inferred from comparative transcriptome analysis of a munidopsid squat lobster distributed in both environments

Oases of life around deep-sea hydrothermal vents and cold seeps have revolutionized our perception of the deep sea. A growing understanding of adaptive strategies for macrofauna living in deep-sea extreme environments has been accompanied by a parallel realization that the species distributed in different types of deep-sea chemosynthetic ecosystems likely require specific adaptation to their respective habitats. Here we put this hypothesis to a test through comparing muscle and hepatopancreas transcriptional profiles of a munidopsid squat lobster, Munidopsis lauensis, from a hydrothermal vent in the Manus back-arc Basin (HV) and a methane seep in the South China Sea (MS). In total, 6680 differentially expressed transcripts (DETs) were identified between HV and MS lobsters, with 3013 DETs specific to the muscle, 2650 DETs specific to the hepatopancreas, and 1017 DETs common to both tissues. The tissue-specific DETs in the muscle were mostly enriched in cytoskeleton and muscle cell development, while those in the hepatopancreas largely functioned in lipid transport and binding. Functional annotation and enrichment analyses revealed the 1017 shared DETs were involved in many biological processes, including detoxification, oxidative stress resistance and innate immune response. Meanwhile, there was clear evidence for the upregulation of genes associated with hydrogen sulfide (H2S) oxidation, endogenous H2S production and mitochondrial oxidative phosphorylation in HV lobsters. This variation in gene expression could have functional relevance for M. lauensis to cope with environmental heterogeneity between HV and MS, such as different concentrations of H2S and heavy metals. Altogether, our results add to previous findings in suggesting that adaptation to deep-sea vent and seep environments involves modification of multiple, complex physiological processes that govern differences in stress resistance.