Adaptive traits for chitin utilization in the saprotrophic aquatic chytrid fungus <i>Rhizoclosmatium globosum</i>

The Chytridiomycota (chytrids) are early diverging fungi, many of which function in ecosystems as saprotrophs; however, associated adaptive traits are poorly understood. We focused on chitin degradation, a common ecosystem function of aquatic chytrids, using the model chitinophilic <i>Rhizoclosmatium globosum</i> and comparison of other chytrid genomes. Zoospores are chemotactic to the chitin monomer <i>N-</i>acetylglucosamine and accelerate development when grown with chitin. The <i>R. globosum</i> secretome is dominated by different glycoside hydrolase (GH) family GH18 chitinases, with abundance matching reciprocal transcriptome mRNA sequences. Models of the secreted chitinases indicate a range of sizes and domain configurations. Along with <i>R. globosum</i>, the genomes of other chitinophilic chytrids also have expanded inventories of GH-encoding genes responsible for chitin processing. Several <i>R. globosum</i> GH18 chitinases have bacteria-like chitin-binding module domains, also present in the genomes of other chitinophilic chytrids yet absent in non-chitinophilic chytrids. Chemotaxis, increased abundance and diversity of secreted chitinases, complemented with the acquisition of novel chitin-binding capability, are probably adaptive traits that facilitate chitin saprotrophy. Our study reveals the underpinning mechanisms that have supported the niche expansion of some chytrids to utilize lucrative chitin-rich particles in aquatic ecosystems and is a demonstration of the adaptive ability of this successful fungal group.