Uncovering thousands of endosymbiont DNA transfer events within single cockroach genomes.

Abstract

Horizontal gene transfer (HGT) between organisms can be a valuable source of genetic variation and innovation. Research on HGT in eukaryotes has hitherto focused on transfers of coding sequences; insertions of noncoding DNA remain poorly understood. Here, we investigated HGT in cockroaches, which have a long-standing evolutionary relationship with the transovarially transmitted endosymbiont <i>Blattabacterium cuenoti</i>, making them a valuable system for assessing the potential scale of HGT. We aligned 150-bp genomic fragments of <i>B. cuenoti</i> to 23 cockroach and termite genomes, including 8 genomes newly sequenced, and revealed pervasive endosymbiont DNA transfer events. Australian panesthiine and geoscapheine cockroaches were consistently found to harbor >3000 HGT inserts, more than an order of magnitude higher than the previous maximum estimate in other eukaryotes, excluding rotifers. Some inserts appear to have persisted for ≥28.7 million years in this group, which may reflect functional roles. We identified numerous chimeric inserts comprising up to nine short segments from different locations in the <i>B. cuenoti</i> genome. Our findings indicate pervasive HGT in eukaryote genomes, with potentially far-reaching implications for adaptation and speciation.