The Melolontha melolontha pathogens Beauveria brongniartii and Beauveria pseudobassiana exhibit clonal genomic population structure in a European Alpine region

Beauveria brongniartii is a fungal pathogen of Melolontha melolontha, a European agricultural pest. Studies have focused on its use to control M. melolontha, however, the B. brongniartii population genomic structure remained unknown and particularly whether this structure is affected by its interaction with M. melolontha, timing of beetle swarming flights, geography or reproductive mode. Therefore, genome-wide SNP-polymorphisms were analyzed to infer the population genomics of Beauveria spp. isolated from M. melolontha adults in an Alpine region. Unexpectedly, only one-third of the isolates were B. brongniartii, whereas two-thirds were apportioned among cryptic taxa within B. pseudobassiana, this far unrecognized as M. melolontha pathogen. Given the prevalence of B. pseudobassiana, analyses were conducted on both species. No spatial or temporal genomic patterns were detected and no correlations were found with M. melolontha population structure, suggesting that fungal dispersal is independent of the beetle. Both species displayed clonal population structures, with B. brongniartii fixed for one mating type and B. pseudobassiana exhibiting both mating types, implying other factors than mating compatibility limiting sexual reproduction. We conclude that B. pseudobassiana has potential as control agent of M. melolontha adults and that Beauveria spp. genomic structure is mainly affected by asexual reproduction and long-distance dispersal.

布氏白僵菌（Beauveria brongniartii）是欧洲农业害虫大栗鳃金龟（Melolontha melolontha）的真菌病原物。过往研究多聚焦于其对大栗鳃金龟的生物防治应用，然而布氏白僵菌的种群基因组结构此前仍未明确，尤其不清楚该结构是否会受到其与宿主的互作、金龟群集飞行时间、地理分布或生殖方式的影响。为此，本研究对阿尔卑斯山区从大栗鳃金龟成虫体内分离得到的白僵菌属（Beauveria spp.）菌株开展全基因组单核苷酸多态性（SNP, Single Nucleotide Polymorphism）分析，以解析其种群基因组学特征。出乎意料的是，仅三分之一的分离菌株为布氏白僵菌，剩余三分之二均隶属于假球孢白僵菌（Beauveria pseudobassiana）类群下的隐蔽分类单元，这类类群此前从未被认定为大栗鳃金龟的病原真菌。鉴于假球孢白僵菌的检出占比更高，本研究对两个物种均开展了后续分析。研究未检测到空间或时间维度的基因组分布模式，也未发现其与大栗鳃金龟种群结构存在相关性，这表明白僵菌的扩散与金龟宿主无关。两个物种均呈现克隆型种群结构：布氏白僵菌仅固定存在一种交配型，而假球孢白僵菌则同时具备两种交配型，这暗示除交配亲和性外，尚有其他因素限制了有性生殖的进行。本研究最终得出结论：假球孢白僵菌具备作为大栗鳃金龟成虫生物防治制剂的潜力，且白僵菌属的基因组结构主要受无性生殖与长距离扩散的影响。