Pawłowska, J. | Search bioRxiv

bioRxiv2021

Horizontal gene transfer in 44 early diverging fungi favors short, metabolic, extracellular proteins from associated bacteria

Numerous studies have been devoted to individual cases of horizontally acquired genes in fungi. It has been shown that such genes expand the hosts metabolic capabilities and contribute to their adaptations as parasites or symbionts. Some studies have provided an extensive characterization of the horizontal gene transfer (HGT) in Dikarya. However, in the early diverging fungi (EDF), a similar characterization is still missing. In order to fill this gap, we have designed a computational pipeline to obtain a statistical sample of reliable HGT events with a possibly minimal number of false detections. We have analyzed 44 EDF proteomes and identified 829 xenologs in fungi ranging from Chytridiomycota and Blastocladiomycota to Mucoromycota. We have identified several patterns and statistical properties of EDF HGT. Ancestrally aquatic fungi are generally more likely to acquire foreign genetic material than terrestrial ones. Endosymbiotic bacteria can be a source of useful xenologs, as exemplified by NOD-like receptors transferred to Mortierellomycota. Closely related fungi have similar rates of intronization of xenologs. The number of post-transfer paralogs of a protein can be described by a heavy-tailed Yule-Simons distribution. Post-transfer gene fusions complicate the landscape of HGT. We have designed a methodology to obtain a reliable, statistical sample of inter-kingdom xenologs across the tree of life of EDF to give a preliminary characterization of their general properties and patterns. We show that HGT is driven by bursts of gene exchange and duplication, resulting in highly divergent numbers and molecular properties of xenologs between fungal lineages. A close ecological relationship with another organism seems to be a predisposing condition for HGT, but does not always result in an extensive gene exchange. We argue that there is no universal approach for HGT identification and inter- and intra kingdom transfers require tailored identification methods. Our results help to better understand how and to what extent HGT has shaped the metabolic, adaptive, and immune capabilities of fungi.

genomics↗

bioRxiv2020

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

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.

genomics↗