The First Complete Mitochondrial Genome of Sarcomyxa edulis (Agaricales): Genomic Characterization and Comparative Analysis with 23 Additional Agaricales Species

Sarcomyxa edulis (Sarcomyxaceae, Agaricales) is an economically important edible and medicinal mushroom native to Northeast Asia. Although its nuclear genome and transcriptomic profiles have been characterized, its mitochondrial genome remains unexplored, hindering a comprehensive understanding of its evolutionary dynamics and phylogenetic placement within Agaricales. The complete mitochondrial genome of S. edulis was assembled using PacBio HiFi long-read sequencing technology. The mitogenome comprises a circular molecule of 248,416 bp with a GC content of 28.02%, exceeding the typical size range of most Agaricales mitogenomes. A total of 51 genes were identified, including 15 PCGs (14 conserved core PCGs plus rps3), 34 tRNA genes, and two rRNA genes; in addition, 153 ORFs were predicted. Genome expansion was primarily attributed to the proliferation of intergenic regions (61.15%) and intronic sequences (30.14%). Codon usage analysis revealed a pronounced preference for AT-rich codons, consistent with the overall nucleotide composition bias. A total of 976 repetitive elements were identified, comprising 465 simple sequence repeats, 216 tandem repeats, and 295 dispersed repeats. Comparative analyses with 23 additional Agaricales species showed that S. edulis possesses one of the largest mitogenomes in Agaricales, with an extensive intron content (40 introns; 12 in cox1, 8 in cob and 7 in cox2), abundant repetitive elements (976; 465 SSRs, 216 tandem repeats and 295 dispersed repeats), a non-coding fraction exceeding 91% (intergenic 61.15% and intronic 30.14%), and a unique gene order (rrn23-cox3-atp8-nad2-nad3-atp9-rrn16-cox1-cox2-nad6-nad4L-nad5-nad4-rps3-cob-nad1-atp6), distinguishing it from other Agaricales mitogenomes. Ka/Ks analysis indicated that all core PCGs are predominantly subject to purifying selection, with atp6, cox3, and nad5 exhibiting the highest nucleotide divergence. Phylogenetic reconstruction based on concatenated mitochondrial PCGs recovered S. edulis as the sister lineage to the Mycena clade, but with weak support (BS = 49%). This placement should therefore be regarded as tentative, and the single Sarcomyxaceae representative analyzed here limits the resolution of family-level relationships within Agaricales. This study provides the first comprehensive characterization of the S. edulis mitogenome, yielding valuable genomic resources for elucidating the evolution and phylogenetics of this commercially important fungus and the underexplored family Sarcomyxaceae. The distinctive genomic features, including an extensive intron content, atypical gene order, and abundant repetitive elements, highlight the dynamic nature of mitochondrial genome evolution in Agaricales.