Clonal evolution and genome stability in a 2500-year-old fungal individual

Abstract

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 rhizomorphs. 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 approximately 75 hectares of the forest floor. Based on observed growth rates of the fungus, we estimate the minimum age of the large individual as 2500 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 unknown at that time. The large individual of A. gallica has been remarkably resistant to genomic change as it has persisted in place.

Syncytia in Fungi

“…The Kingdom Fungi contains some of the longest-living organisms on the planet. The ‘humongous fungus’, or Armillaria gallica , is an example of a fungal syncytium that has lived for over 2500 years, covers 37 hectares, and weighs more than 4 × 10 5 kg [ 57 ]. Even through time and distance, the genetic makeup of this single A. gallica colony has remained surprisingly stable.…”

Somatic mutations and genome stability maintenance in clonal coral colonies

“…Higher per-mitosis mutation rate in mice than humans have been proposed as an explanation for 381 differences in the lifespan of the two species (Milholland et al 2017). Lack of information about 382 cell division rates proves to be a consistent problem in estimating mutations rates of many non-383 model organisms, including spruce trees (Hanlon et al 2019), and another long-lived clonal 384 organism, the fungus Armillaria gallica (Anderson et al 2018). More work on rates of cell 385 division in coral adults, in addition to sampling strategies that explicitly take distance and 386 positioning between samples into account, will determine whether corals have a low rate of 387 mutation per cell division.…”

Native and invasive populations of the ectomycorrhizal death capAmanita phalloidesare highly sexual but dispersal limited

“…Basidiospores may give rise to relatively small mycelia that persist for short periods of time before reproducing sexually. Life history evolution among fungi is poorly described (a stark contrast to traditions within the plant literature; Harper 1977; Grime 1977) but A. phalloides emerges in stark contrast to the “humongous fungus,” epitomized by the pathogens Armillaria gallica (Anderson et al ., 2018) and A. ostoyae (Shaw & Roth, 1976; Ferguson et al ., 2003). The death cap appears to persist in habitats as a small bodied, ephemeral, potentially ruderal species.…”

“…Steady vegetative growth can result in enormous mycelia (e.g., Armillaria spp. ), but whether fragmentation enables colonization of empty habitats is often unclear (Smith et al ., 1992; Anderson et al ., 2018).…”