Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Abstract

Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. The genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata - M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.

Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina

“…A phylogeny based on a concatenation of 784 single‐copy, orthologous protein sequences (Fig. ) strongly supports the erection of Mucoromycota to unite Glomeromycotina, Mortierellomycotina and Mucoromycotina (Spatafora et al ., ; Uehling et al ., ).…”

“…The functional genomic comparison made through KEGG pathway profile correlations (Fig. b) also showed that the sequenced Glomeromycotina present a higher metabolic similarity between taxa compared to M. elongata /Mucoromycota species, corroborating and extending M. elongata genome analysis (Uehling et al ., ). Lack of PCWDE (see next section), degradation of sucrose and glycogen (i.e.…”

“…For each category, we also identified single‐copy and duplicated genes. As expected for species that diverged > 450 Ma (Uehling et al ., ), clustering of the predicted protein sequences of the eight Mucoromycota led to a very restricted core set of genes (Fig. ; Table S3).…”

“…To assess the orthology between gene sets from the eight species of Mucoromycota sensu Spatafora et al . (), we downloaded gene models of Mortierella elongata AG‐77 v.2.0 (Uehling et al ., ), Mucor circinelloides CBS277 v.2.0 (Corrochano et al ., ), Phycomyces blakesleeanus NRRL1555 v.2.0 (Corrochano et al ., ) and Rhizopus microcarpus ATCC52814 v.1.0 (Lastovetsky et al ., ) from the JGI MycoCosm database. We clustered the predicted proteins of these taxa, together with the present Glomeromycotina predicted proteins, with FastOrtho using 50% identity and 50% coverage (Wattam et al ., ).…”

Bifiguratus adelaidae, gen. et sp. nov., a new member of Mucoromycotina in endophytic and soil-dwelling habitats

“…Recent studies have provided evidence of the presence of bacteria in some Mucoromycotina, such as Endogone, where similar Mollicutes-related endobacteria have been detected (Desirò et al 2015). Endobacteria occur in the cytoplasm of Mortierellomycotina, such as Mortierella elongata (Sato et al 2010;Uehling et al 2017) and Rhizopus (Partida-Martinez and Hertweck 2005). Based on SEM micrographs, we conclude that at least some of these bacteria are epihyphal in B. adelaidae, but additional testing is necessary to determine if any of the bacteria detected on this fungus are endobiotic.…”