Inter‑symbiont horizontal gene transfer and functional partitioning in globally sampled lichen metagenomes

Horizontal gene transfer (HGT) is a fundamental eco‑evolutionary process, yet its functional and symbiotic significance in lichens remains poorly understood. Here, using 197 high‑completeness eukaryotic metagenome-assembled genomes derived from 533 lichen-associated metagenomes sampled across six continents, we detect 1,882 putative HGT‑acquired genes among ~1.6 million predicted genes (~0.12%) across the major symbiotic partners, most of which were of bacterial origin. This dataset enables us to test two hypotheses: (H1) HGT-acquired genes exhibit partner-specific functional profiles consistent with functional differentiation between the major symbiotic partners, and (H2) inter‑symbiont HGT has occurred across the fungal–algal interface. Consistent with H1, putative HGT‑acquired genes in mycobionts show greater representation of functions related to cell wall/membrane/envelope biogenesis, transcription, and defense mechanisms, whereas putative HGT‑acquired genes in photobionts show greater representation of functions related to amino acid transport and metabolism, signal transduction, and translation. Consistent with H2, we detect 31 putative inter‑symbiont HGT-acquired genes (16 inferred from mycobionts to photobionts and 15 inferred from photobionts to mycobionts), including multiple photobiont genes inferred to encode RfeF transcription factors with putative mycobiont origin, suggesting a potential contribution of HGT to regulatory evolution. These findings are consistent with a potential role of HGT in functional specialization and potential gene flow across fungal–algal boundaries, offering insights into the eco‑evolutionary dynamics of symbiotic systems. Horizontal gene transfer may shape how lichen symbionts adapt, but its role remains unclear. Across 197 lichen MAGs, this study identified 1,882 putative horizontally transferred genes and 31 potential transfers between fungal and algal symbionts, with distinct functional patterns.