Metabolic potential, ecology and presence of endohyphal bacteria is reflected in genomic diversity of Mucoromycotina

Abstract

We describe the genomes of six Mucoromycotina fungi representing distant saprotrophic lineages within the subphylum (i.e. Umbelopsidales and Mucorales). We selected two Umbelopsis isolates from soil (i.e. U. isabellina, U. vinacea), two soil-derived Mucor isolates (i.e. M. circinatus, M. plumbeus), and two Mucorales representatives with extended proteolytic activity (i.e. Thamnidium elegans and Mucor saturninus). We complement genome analyses with a description of their digestive capabilities, their cell wall carbohydrate composition, and total lipid profiles. Finally, we link the presence of endohyphal bacteria with observed characteristics. One of the genomes, Thamnidium elegans, harbours a complete genome of an associated bacterium classified to Paenibacillus sp. This fungus displays multiple altered traits compared to remaining isolates regardless of their evolutionary distance. T. elegans has expanded carbon assimilation capabilities particularly efficiently degrades carboxylic acids, has a higher diacylglycerol: triacylglycerol ratio and phospholipid composition suggesting a more rigid cellular membrane. Comparison of early-diverging Umbelopsidales with evolutionary younger Mucorales points at several differences particularly in their carbon source preferences and encoded carbohydrate repertoire. All tested Mucoromycotina shares features including the ability to produce 18:3 gamma-linoleic acid and fucose as a cell wall component. Author SummaryIn our paper, we report on the genomic sequences of six Mucoromycotina strains and an associated bacterium from Paenibacillus genus. Mucoromycotina are often studied in pathogenic context albeit their basic biology remains understudied. This manuscript expands on the collection of currently sequenced Mucorales and Umbelopsidales, including the first sequenced Thamnidium isolate, which was sequenced together with a Paenibacillus bacterium. The interaction with a bacterial partner alters the metabolism, cell membrane composition but not the exoskeleton of the fungus. The associated bacterium provided multiple enzymes that significantly expanded the digestive capabilities of the fungal host. Parallel sequencing and phenotyping of Mucorales and Umbelopsidales enabled us to look at the differences of both lineages within Mucoromycotina. We demonstrate that the predicted digestive capabilities are in line with experimental validation. Based on the cell wall composition data and genomic underpinnings of carbohydrate metabolism we were able to confirm the universal presence of fucose in Mucoromycotina cell walls. Fatty acid, phospholipid and acylglycerol composition support the usage of 18:3 gamma-linoleic acid as a chemotaxonomic marker of Mucoromycotina and corroborate TAG as a dominant storage lipid in these organisms. Genomic features, digestive capabilities, fatty acid composition differ between Mucorales and Ubelopsidales pointing at subtle but significant changes in the course of Mucoromycotina radiation.