Comparative genomics and stable isotope analysis reveal the saprotrophic-pathogenic lifestyle of a neotropical fungus

In terrestrial forested ecosystems, fungi may interact with trees in at least three distinct ways: (i) associated with roots as symbionts; (ii) as pathogens in roots, trunks, leaves, flowers, and fruits; or (iii) decomposing dead tree tissues on soil or even on dead tissues in living trees. Distinguishing the latter two nutrition modes is rather difficult in Hymenochaetaceae (Basidiomycota) species. Herein, we have used an integrative approach of comparative genomics, stable isotopes, host tree association, and bioclimatic data to investigate the lifestyle ecology of the scarcely known neotropical genus <i>Phellinotus</i>, focusing on the unique species <i>Phellinotus piptadeniae</i>. This species is strongly associated with living <i>Piptadenia gonoacantha</i> (Fabaceae) trees in the Atlantic Forest domain on a relatively high precipitation gradient. Phylogenomics resolved <i>P. piptadeniae</i> in a clade that also includes both plant pathogens and typical wood saprotrophs. Furthermore, both genome-predicted Carbohydrate-Active Enzymes (CAZy) and stable isotopes (δ¹³C and δ¹⁵N) revealed a rather flexible lifestyle for the species. Altogether, our findings suggest that <i>P. piptadeniae</i> has been undergoing a pathotrophic specialization in a particular tree species while maintaining all the metabolic repertoire of a wood saprothroph.<h4>Importance</h4>This is the first genomic description for <i>Phellinotus piptadeniae</i>. This basidiomycete is found across a broad range of climates and ecosystems in South America, including regions threatened by extensive agriculture. This fungus is also relevant considering its pathotrophic-saprotrophic association with <i>Piptadenia goanocantha</i>, which we began to understand with these new results that locate this species among biotrophic and necrotrophic fungi.