Massive gene loss in the fungus Sporothrix epigloea accompanied a shift to life in a glucuronoxylomannan-based gel matrix

Abstract Fungi are well known for their ability to both produce and catabolize complex carbohydrates to acquire carbon, often in the most extreme of environments. Glucuronoxylomannan (GXM)-based gel matrices are widely produced by fungi in nature and though they are of key interest in medicine and pharmaceuticals, their biodegradation is poorly understood. Though some organisms, including other fungi, are adapted to life in and on GXM-like matrices in nature, they are almost entirely unstudied, and it is unknown if they are involved in matrix degradation. Sporothrix epigloea is an ascomycete fungus that completes its life cycle entirely in the short-lived secreted polysaccharide matrix of a white jelly fungus, Tremella fuciformis. To gain insight into how S. epigloea adapted to life in this unusual microhabitat, we compared the predicted protein composition of S. epigloea to that of 21 other Sporothrix species. We found that the genome of S. epigloea is smaller than that of any other sampled Sporothrix, with widespread functional gene loss, including those coding for serine proteases and biotin synthesis. In addition, many predicted CAZymes degrading both plant and fungal cell wall components were lost while a lytic polysaccharide monooxygenase (LPMO) with no previously established activity or substrate specificity, appears to have been gained. Phenotype assays suggest narrow use of mannans and other oligosaccharides as carbon sources. Taken together, the results suggest a streamlined machinery, including potential carbon sourcing from GXM building blocks, facilitates the hyperspecialized ecology of S. epigloea in the GXM-like milieu.