Deep-sea megafauna co-opts microbial energy metabolism genes to withstand ultra-long starvation.

Abstract

The deep-sea supergiant isopod is renowned for surviving over 5 years without food, which is a crucial adaptive trait for megafauna inhabiting extreme environments. Here, morphological, physiological, and genomic comparisons of deep-sea isopods reveal a dual adaptive strategy underlying this trait: a distended, food-retentive stomach that enables episodic hyperphagia and a markedly reduced basal metabolic rate (BMR). Notably, central to this adaptation is the ancient horizontal acquisition of the microbial energy metabolism-related gene ND1, which thereafter achieved significant dosage enhancement via post-transfer duplication and ultra-high expression that is specifically regulated by histone acetylation at its promoter. Functional assays in transgenic zebrafish, nematodes, and cell lines demonstrate that ND1 reduces BMR by downregulating endogenous energy-production genes and thus extends starvation survival under cold-induced metabolic suppression. These findings uncover an exceptional evolutionary strategy whereby deep-sea megafauna co-opts and epigenetically optimizes exogenous microbial genes to reconcile the metabolic conflict between energy-demanding gigantism and extreme energy limitation.