Tracing the evolution of shiitake mushrooms

Shiitake mushrooms get their name from the same place where they often get their nutrients – the shii tree, a Japanese relative of the oak. These fungi belong to the genus Lentinula, which has evolved to decompose hardwoods on every continent except Europe and Antarctica.

A new analysis published in Proceedings of the National Academy of Sciences takes a genomic look at Lentinula specimens from around the world. By fully sequencing 24 mushroom genomes and assembling genomes from 60 existing sequences, this work extends the family tree of Lentinula. Within these samples, this study also monitors the enzymes these fungi use to break down the wood and compares the genetic diversity between cultivated and wild shiitake populations.

Lentinula mushrooms are white-rot fungi, belonging to an elite group of decomposers that can break down all components of wood—cellulose, hemicellulose, and the hardest molecule, lignin. Understanding Lentinula genomes and their evolution could provide strategies for converting plant waste into sugars for biofuel production. In addition, these fungi play a role in the global carbon cycle. As decomposers, Lentinula fungi access carbon that was previously locked in the wood, converting it into their own carbon-rich structures, as well as atmospheric carbon dioxide.

The researchers sequenced 11 specimens from Asia-Australia and 13 specimens from the Americas to trace the evolution of Lentinula species. The genus Lentinula diverged about 28 million years ago, when the largest mammal ever, Paraceratherium, still roamed central Asia. The Lentinula groups then evolved further, into four major groups: one lineage in Australia and L aciculospora, L. raphanica and L boryana in the Americas. Tracing these phylogenetic relationships suggests that the shiitake mushroom, Lentinula edodes, originated in the tropics of the Asia-Australia region. Overall, pangenome analysis showed significantly greater genetic diversity in wild Lentinula species compared to domesticated varieties, highlighting a potential conservation threat to wild species.

Sequencing between genomes also provided an opportunity to assess commonalities. The enzymes that Lentinula fungi rely on to decompose wood were broadly conserved across species. In particular, many species had very similar plant cell wall degrading enzymes (PCWDEs), including carbohydrate-active enzymes, oxidoreductases, and cytochrome P450s. This includes the species L. raphanica, which has managed to adapt to habitats from Alabama to Brazil, suggesting that the same enzymes associated with decomposition are useful in a wide range of environments.

The collection and analysis of these samples was a global collaboration that brought together 39 researchers from eight different countries. Genome and transcriptome sequencing was enabled by the Community Science Program (CSP) at the US Department of Energy’s (DOE) Joint Genome Institute (JGI), a DOE science office user facility located at Lawrence Berkeley National Laboratory (Berkeley Lab ).