Clonal evolution and genome stability in a 2,500-year-old fungal individual

Individuals of the basidiomycete fungus Armillaria are well-known for their ability to spread from woody substrate to substrate on the forest floor through the growth of rhizomoprhs. Here we made 248 collections of A. gallica in one locality in Michigan’s Upper Peninsula. To identify individuals, we genotyped collections with molecular markers and somatic compatibility testing. We found several different individuals in proximity to one another, but one genetic individual stood out as exceptionally large, covering hundreds of tree root systems over approximate 75 hectares of forest floor. Based on observed growth rates of the fungus, we estimate the minimum age of the large individual as 2,500 years. With whole-genome sequencing and variant discovery, we also found that mutation had occurred within the somatic cells of the individual, reflecting its historical pattern of growth from a single point. The overall rate of mutation over the 90 mb genome, however, was extremely low. This same individual was first discovered in the late 1980s, but its full spatial extent and internal mutation dynamic was unkown at that time. The large individual of A. gallica has been remarkably resistant to genomic change as it has persisted in place.

蜜环菌属（Armillaria）担子菌的个体，凭借可通过根状菌索（rhizomorphs）生长在林地地表的木质基质间扩散的能力而广为人知。本研究于美国密歇根州上半岛的一处样地中，采集了248份高卢蜜环菌（Armillaria gallica）标本。为界定真菌个体单元，我们通过分子标记基因分型与体细胞兼容性测试对采集的标本进行了鉴定。研究发现多个不同的真菌个体彼此邻近分布，但其中一个遗传个体体型格外庞大，覆盖了约75公顷林地地表内的数百个树木根系。基于该真菌已观测到的生长速率，我们估算该大型个体的最小存续年龄为2500年。通过全基因组测序与变异检测，我们还发现该个体的体细胞内发生了突变，这反映了其从单一起始点逐步扩张的生长历史模式。不过，其90兆碱基（Mb）的基因组整体突变率极低。该个体最早于20世纪80年代末被发现，但当时人们尚未明确其完整空间分布范围与内部突变动态。这株高卢蜜环菌的大型个体在持续留存于原地的过程中，展现出了极强的基因组稳定性。