Expanded mushroom genomes with versatile adaptability

Independent genome expansion in Mycena s.s. unaffected by plant hosts or substrates.

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A study published in Cell Genomics reveals that various Mycena mushroom species possess unexpectedly large genomes. Previously believed to be purely saprotrophic—degrading dead organic matter—the mushrooms possess diverse genes enabling them to adapt to different lifestyles. Notably, Mycena strains in Arctic regions exhibit some of the most giant mushroom genomes recorded.

These mushrooms display extensive genome expansion, encompassing genes for interacting with plants, carbon breakdown, and potentially vital yet unidentified functions. They also contain repetitive non-coding elements and genes acquired through horizontal gene transfer from unrelated fungi.

Dr. Shingo Miyauchi from the Okinawa Institute of Science and Technology (OIST) explained that Mycena samples collected in Northern Europe, including Arctic regions, showed significantly larger genomes than typical Mycena species. Collaborators verified these findings, confirming the uniqueness of these expanded genomes in Arctic Mycena species.

Francis Martin from INRAE and the University of Lorraine highlighted that despite the costs, the large genomes of these Arctic Mycena fungi likely provide adaptability and versatility. This evolutionary advantage is crucial in extreme environments like the Arctic, similar to plant observations.

Image showing Mycena mushrooms exhibit extensive genomic expansion, encompassing not only the genes facilitating plant invasion, carbon breakdown, and interaction, but also those with yet unknown but likely significant functions.
Mycena mushrooms exhibit extensive genomic expansion, encompassing not only the genes facilitating plant invasion, carbon breakdown, and interaction, but also those with yet unknown but likely significant functions. Credit: Arne Aronsen and Christoffer Harder

The researchers aimed to study Mycena, a key decomposer of forest litter, and their role in the carbon cycle. Despite their small size, Mycena plays a crucial role in ecosystems. Previously thought to feed solely on dead organic matter, some Mycena species were discovered to also interact with living plants.

Mycena are also known for their bioluminescence. Earlier studies on five Mycena species explored their genomes to understand this trait. The researchers expanded their study to include 24 additional Mycena species and one related species, Atheniella floridula, which have varied preferences for substrates like wood and leaf litter. They compared these genomes with 33 from other species to explore evolutionary changes and differences in enzymes that break down plant cell walls based on their lifestyles.

The researchers found that Mycena mushrooms have significantly larger genomes than expected, affecting all gene families regardless of their typical behaviors. This expansion was driven by new gene emergence, gene duplications, increased enzyme-producing genes for breaking down plant material, more transposable elements, and genes transferred horizontally from other fungi.

Two Arctic species had the most giant genomes, much bigger than temperate zone Mycena, surprising the researchers. They also discovered genes from Ascomycetes transferred into Mycena, including species from temperate regions, suggesting unclear reasons for their large size, possibly linked to Arctic conditions.

In Arctic plants, genomes can expand through transposable elements or complete duplication compared to relatives in temperate zones. Similar evolutionary patterns might be occurring in Arctic mushrooms.

Håvard Kauserud from the University of Oslo suggests that Mycena mushrooms show a real-time transition from decomposing to forming symbiotic relationships, a process believed to have happened millions of years ago in other fungal groups.

Christoffer Bugge Harder, also from the University of Oslo, notes that, unlike many other fungi, Mycena can adopt various lifestyles. This flexibility is reflected in their genome structures.

The findings also highlight challenges in interpreting an organism’s behavior solely from its genome.

Dr. Miyauchi, a data scientist passionate about visual art, found inspiration in the colors of tiny mushrooms while comparing fungal genome features for the study. Influenced by 19th-century French impressionist Pierre-Auguste Renoir, he created figures.

Currently, Dr. Miyauchi focuses on sequencing genomes of rare deep-sea fungi, which differ significantly from forest fungi. His goal is genome mining to uncover unique genes, enzymes, and metabolites for future biotechnological applications. Dr. Miyauchi hopes funding bodies recognize the vast potential of these tiny mushrooms.

Journal reference:

  1. Christoffer Bugge Harder, Shingo Miyauchi, et al., Extreme overall mushroom genome expansion in Mycena s.s. irrespective of plant hosts or substrate specializations. Cell Genomics. DOI: 10.1016/j.xgen.2024.100586.

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