Telomere-to-telomere genome assembly of Metarhizium acridum provides insights into Metarhizium genome evolution

Metarhizium acridum is a highly specialized entomopathogenic fungus widely used as a biocontrol agent against locusts. Despite its ecological and agricultural importance, the genomic basis of its host specificity and pathogenicity remains poorly understood. We present the first telomere-to-telomere (T2T) genome assembly of M. acridum, using PacBio HiFi sequencing and Hi-C scaffolding data, for seven chromosomes (45.1 Mb, N50 = 5.9 Mb) with 96.7% BUSCO completeness, which is the most contiguous Metarhizium genome to date. Repeat elements constitute 19.7% of the genome, dominated by long terminal repeat (LTR) retrotransposons (8.6%) while genome annotation revealed 11,623 protein-coding genes, including 716 carbohydrate-active enzymes and 254 effector proteins. Comparative genomics analysis identified 257 genes shared between M. acridum and M. anisopliae, 465 genes shared between M. acridum and M. brunneum. Synteny analysis indicated frequent chromosomal rearrangements between M. acridum and M. brunneum, with fragments from one chromosome of M. acridum distributed to 2–6 chromosomes of M. brunneum. The aegerolysin-domain toxin gene MaAh-1A showed approximately 10-fold upregulation during locust infection. After trypsin-activated of MaAh-1A, an approximately 16% decline of survival rate was observed. Our study provides an ideal reference T2T genome as the foundational resource for exploring genomic resources of biological control and advancing the application of Metarhizium fungi in sustainable pest management.