Extensive horizontal gene transfer drives microbial adaptation and diversification in Kermadec Trench hadal microbiomes.

Hadal trenches, plunging beyond six kilometers depth, harbor a dynamic yet enigmatic microbial biosphere. From ~10 km depth Kermadec Trench sediments, we integrated metagenomics, in situ metatranscriptomics, and phylogenetics to reconstruct 300 prokaryotic species and 186,496 viral populations. In hadal sediment metagenomes analyzed here, we detect distant horizontal gene transfer (DHGT) across phyla/domains and estimate that it contributes on average ~13% of each genome and accounting for >46.7% of multi-copy gene expansions, with four phyla acquiring more than 30% of their genes via DHGT. These DHGT genes encode critical adaptations, including reactive oxygen species detoxification, aromatic compound degradation, and fatty acid/heme biosynthesis, which help microbes survive extreme pressure, low temperatures, and oligotrophy. While classical mechanisms such as conjugation (~0.27%), transduction (~2.1%), and transformation account for a fraction of events, additional potential gene flow conduits are proposed: magnetotaxis-mediated encounters by magnetotactic bacteria (~17.4% of DHGT events), possibly increasing opportunities for gene exchange. These findings suggest that DHGT can contribute substantially to metabolic diversification in the hadal genomes, representing an evolutionary mode distinct from gradualist Darwinian inheritance and consistent with the idea that episodic acquisition of functional modules can contribute to rapid metabolic diversification.