Transcriptional responses of the lower lip of Colossoma macropomum: An adaptation to aquatic surface respiration under hypoxic conditions

Colossoma macropomum, a fish native to the Amazon with high ecological and economic importance, has become the principal regional model for studying adaptive strategies to low-oxygen environments. To elucidate the molecular mechanisms underlying hypertrophy and expansion of the lower lip in C. macropomum, we performed a transcriptomic analysis under both hypoxic and normoxic conditions. We identified 1,704 genes with increased expression and 1,090 with decreased expression, while 27,475 genes showed no differential expression. The results indicate that the HIF pathway plays a crucial role in the development of the lower lip in C. macropomum, as stabilization of HIF-1α/HIF-1β promotes the expression of genes associated with angiogenesis, metabolic adjustments, and tissue and vascular remodeling. Evidence also indicates that lip expansion involves more than the increase in volume, can be associated with the formation of a complex vascular network, similar to the gills and auxiliary respiratory systems of other teleosts. As a metabolic adaptation, lip cells in C. macropomum undergo modifications in cellular transport mechanisms, including downregulation of aerobic metabolite transport systems and upregulation of glycolytic pathways. These findings indicate that lip expansion results from regulated hypertrophy, remodeling of the extracellular matrix, and epithelial-mesenchymal interactions rather than from uncontrolled cell proliferation. This mechanism helps to explain the functional and reversible nature of lip expansion.