Divergent evolution of early terrestrial fungi reveals the evolution of Mucormycosis pathogenicity factors

Abstract

Fungi have evolved over millions of years and their species diversity is predicted to be the second largest on the earth. Fungi have cross-kingdom interactions with many organisms which have mutually shaped their evolutionary trajectories. Zygomycete fungi hold a pivotal position in the fungal tree of life and provide important perspectives on the early evolution of fungi from aquatic to terrestrial environments. Phylogenomic analyses have found that zygomycete fungi diversified into two separate clades, the Mucoromycota which are frequently associated with plants and Zoopagomycota that are commonly animal-associated fungi. Genetic elements that contributed to the fitness and divergence of these lineages may have been shaped by the varied interactions these fungi have had with plants, animals, bacteria and other microbes. To investigate this, we performed comparative genomic analyses of the two clades in the context of Kingdom Fungi, benefiting from our generation of a new collection of zygomycete genomes. We identified lineage-specific genomic content which may contribute to the disparate biology observed in these zygomycetes. Our findings include the discovery of undescribed diversity in CotH, a Mucormycosis pathogenicity factor, which was found in a broad set of zygomycetes. Reconciliation analysis identified multiple duplication events and an expansion of CotH copies throughout Mucoromycotina, Mortierellomycotina, Neocallimastigomycota, and Basidiobolus lineages. A kingdom-level phylogenomic analysis also identified new evolutionary relationships within the sub-phyla of Mucoromycota and Zoopagomycota.

Prevalence and diversity of TAL effector-like proteins in fungal endosymbiotic Mycetohabitans spp.

“…Using long-reads, we sequenced and assembled seven new Mycetohabitans genomes and re-sequenced two of the three previously sequenced genomes, and examined the encoded Btl protein sequences to determine their distribution, diversity and evolutionary relationships. To expand this analysis, we also mined deep, short-read holobiont contig assemblies for a large collection of fungal isolates from the ZygoLife project (Joint Genome Sequencing Project doi: 10.46936/10.25585/60001062) [18,[26][27][28]. Here we report the findings of this two-part approach, 46 Btl proteins and 48 btl gene fragments from Mrh and Mef genomes, revealing widespread distribution and substantial variation in sequence and predicted DNA binding specificity, as well as species-specific patterns of conservation.…”

“…To explore Btl protein diversity more fully, we probed fungal genome sequencing data from the ZygoLife Project which aimed to understand taxonomic diversity and evolutionary history of the Mucoromycota and Zoopagomycota fungi [18,27,28,[54][55][56][57].…”

Prevalence and diversity of TAL effector-like proteins in fungal endosymbiotic Mycetohabitans spp.

“…Using long-reads, we sequenced and assembled seven new Mycetohabitans genomes and re-sequenced two of the three previously sequenced genomes, and examined the encoded Btl protein sequences to determine their distribution, diversity, and evolutionary relationships. To expand this analysis, we also mined deep, short-read holobiont contig assemblies for a large collection of fungal isolates from the ZygoLife project (Joint Genome Sequencing Project doi: 10.46936/10.25585/60001062) (19)(20)(21)(22). Here we report the findings of this two-part approach, 46 Btl proteins and 48 btl gene fragments from Mrh and Mef genomes, revealing widespread distribution and substantial variation in sequence and predicted DNA binding specificity, as well as species-specific patterns of conservation.…”