Genome reshuffling as a route to specialization? Chromosome-level insights from the bark beetle symbiont genus Geosmithia.

Abstract

Evolution of genome architecture is increasingly recognized as a major driver of fungal adaptation. However, because most studies have focused on plant and human pathogens, the genomic mechanisms underlying adaptation beyond pathogenic lifestyles remain poorly understood. Here, we establish the bark beetle-associated fungal genus Geosmithia as a model for studying genome evolution during ecological transitions. Geosmithia species occupy diverse ecological niches ranging from generalists, facultative symbionts of multiple beetle vectors and host tree species to more specialized conifer specialists and obligate nutritional symbionts of ambrosia beetles. Using chromosome-level genome assemblies of eleven species representing independently evolved ecological strategies, we investigated how genome architecture, repetitive DNA, and gene family evolution contribute to this ecological diversification. Comparative genomics revealed pervasive intra- and interchromosomal rearrangements, even between recently diverged species, demonstrating that extensive chromosome restructuring can accumulate over short evolutionary timescales. Breakpoints frequently occurred in gene-rich rather than repeat-rich regions, contrasting with the transposable element-associated patterns commonly described in fungi. Hi-C analyses revealed a typical Rabl chromosome organization but highly unusual centromeres that are repeat-poor, gene-rich, transcriptionally active, and conserved as syntenic blocks across species. Further, centromere identity may be determined by a highly divergent CenH3 variant. Despite similar genome sizes, specialists had increased repetitive DNA content and widespread gene family contractions, consistent with metabolic streamlining during ecological specialization. Our results demonstrate that extensive structural genome evolution can occur in gene-dense fungal genomes and establish Geosmithia as a powerful model for studying the interplay between genome evolution and ecological diversification.