Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Chang, Ying; Wang, Yan; Mondo, Stephen J.; Ahrendt, Steven; Andreopoulos, William; Barry, Kerrie; Beard, Jeff; Benny, Gerald L.; Blankenship, Sabrina; Bonito, Gregory; Cuomo, Christina A.; Desirò, Alessandro; Gervers, Kyle A.; Hundley, Hope; Kuo, Alan; LaButti, Kurt; Lang, B. Franz; Lipzen, Anna; O’Donnell, Kerry; Pangilinan, Jasmyn; Reynolds, Nicole; Sandor, Laura; Smith, Matthew; Tsang, Adrian; Grigoriev, Igor V.; Stajich, Jason E.; Spatafora, Joseph W.

doi:10.1016/j.isci.2022.104840

Cited by 23 publications

(22 citation statements)

References 62 publications

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“…The former taxonomic unit, Zygomycota, has been recognized paraphyletic and thus been abandoned and replaced by Mucoromycota and Zoopagomycota to accommodate the six major lineages—Glomeromycotina, Mortierellomycotina, Mucoromycotina, Entomophthoromycotina, Kickxellomycotina, and Zoopagomycotina ( James, Kauff, et al 2006 ; White et al 2006 ; Hibbett et al 2007 ; Spatafora et al 2016 ). Since the loss of flagella, the first evolutionary split of terrestrial fungi leads to Zoopagomycota and the clade of Mucoromycota and Dikarya ( Chang et al 2021 ). Mucoromycota is the sister clade of the subkingdom Dikarya clades (Ascomycota and Basidiomycota) ( figs.…”

Section: Discussionmentioning

confidence: 99%

“…Zygomycete fungi are a historically enigmatic group as their diversity and phylogenetic placement on the fungal tree of life remained somewhat cryptic based on morphological characters alone. The lineages emergence coincides with major transition of fungi from aquatic environment to terrestrial ecologies, which was characterized by the evolutionary loss of the flagellum ( James, Kauff, et al 2006 ; James, Letcher, et al 2006 ; Chang et al 2021 ). The zygomycete fungi are recognized by their gametangial conjugation, production of zygospore, and coenocytic aseptate or septate hyphae ( White et al 2006 ; Hibbett et al 2007 ; Spatafora et al 2017 ; Naranjo-Ortiz and Gabaldón 2020 ).…”

Section: Introductionmentioning

confidence: 99%

“…Zygomycete fungi were found to be paraphyletic based on genome-scale evidence; as a result, two new phyla (Mucoromycota and Zoopagomycota) were established to accommodate the current members ( Spatafora et al 2016 ). However, incomplete sampling of zygomycete lineages has made resolution of the origin of terrestrial fungi difficult to resolve with standard phylogenetic approaches ( Chang et al 2021 ; Li et al 2021 ).…”

Section: Introductionmentioning

confidence: 99%

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Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Wang

Chang

Ortañez

et al. 2023

Genome Biology and Evolution

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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 of zygomycetes in the context of Kingdom Fungi, benefiting from our generation of a new collection of zygomycete genomes, including nine produced for this study. 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 the Mucoromycotina, Mortierellomycotina, Neocallimastigomycota, and Basidiobolus lineages. A kingdom-level phylogenomic analysis also identified new evolutionary relationships within the sub-phyla of Mucoromycota and Zoopagomycota, including supporting the sister-clade relationship between Glomeromycotina and Mortierellomycotina and the placement of Basidiobolus as sister to other Zoopagomycota lineages.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Wang

Chang

Ortañez

et al. 2023

Genome Biology and Evolution

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“…However, technological advances such as single-cell genome sequencing have generated additional data for challenging parasitic taxa ( Ahrendt et al 2018 ; Davis et al 2019 ). Genome-scale data have also facilitated new insights into the biology of Zoopagomycota fungi by elucidating metabolic pathways and secondary metabolite production ( Ahrendt et al 2018 ; Tabima et al 2020 ), the evolution of plant cell wall degrading enzymes and small secreted proteins ( Chang et al 2015 , 2022 ), and horizontal gene transfer events ( Tabima et al 2020 ; Wang et al 2016a ). Zoopagomycota are further divided into three subphyla: Entomophthoromycotina (insect parasites), Zoopagomycotina (parasites of fungi and small animals such as nematodes), and Kickxellomycotina (several trophic strategies, see below) ( Hibbett et al 2007 ; Spatafora et al 2016 ).…”

Section: Introductionmentioning

confidence: 99%

“…We do not include the number of reads per base in our definition due to the small expected genome size of our species; therefore, we anticipate high reads per base coverage that may not correspond to a high-quality assembly (e.g., low BUSCO complete scores, large number of contigs). The quality of assembly can also depend on the repetitive sequence content, which is quite low for the Kickellomycotina (2–6%) ( Ahrendt et al 2018 ; Amses et al 2022 ; Chang et al 2015 ; Chang et al 2022 ; Mondo et al 2017 ; Wang et al 2016a , 2016b ). There are several conditions under which LGCS would be a more appropriate choice than other genome sequencing methods, including: 1) phylogenetic reconstruction is the main goal of data analysis, 2) the genome sizes of the target species are small and high coverage can be achieved with short read sequencing, and 3) many isolates will be sequenced (and therefore cost is an important consideration).…”

Section: Introductionmentioning

confidence: 99%

Mycoparasites, Gut Dwellers, and Saprotrophs: Phylogenomic Reconstructions and Comparative Analyses of Kickxellomycotina Fungi

Reynolds

Stajich

Benny

et al. 2023

Genome Biology and Evolution

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Improved sequencing technologies have profoundly altered global views of fungal diversity and evolution. High throughput sequencing methods are critical for studying fungi due to the cryptic, symbiotic nature of many species, particularly those that are difficult to culture. However, the low coverage genome sequencing (LCGS) approach to phylogenomic inference has not been widely applied to fungi. Here we analyzed 171 Kickxellomycotina fungi using LCGS methods to obtain hundreds of marker genes for robust phylogenomic reconstruction. Additionally, we mined our LCGS data for a set of nine rDNA and protein coding genes to enable analyses across species for which no LCGS data were obtained. The main goals of this study were to: 1) evaluate the quality and utility of LCGS data for both phylogenetic reconstruction and functional annotation, 2) test relationships among clades of Kickxellomycotina, and 3) perform comparative functional analyses between clades to gain insight into putative trophic modes. In opposition to previous studies, our nine-gene analyses support two clades of arthropod gut dwelling species and suggest a possible single evolutionary event leading to this symbiotic lifestyle. Furthermore, we resolve the mycoparasitic Dimargaritales as the earliest diverging clade in the subphylum and find four major clades of Coemansia species. Finally, functional analyses illustrate clear variation in predicted carbohydrate active enzymes and secondary metabolites (SM) based on ecology, i.e., biotroph vs. saprotroph. Saprotrophic Kickxellales broadly lack many known pectinase families compared to saprotrophic Mucoromycota and are depauperate for SM but are enriched for chitinases compared to biotrophic taxa in Zoopagomycota.

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Biotransformation of fluorinated drugs and xenobiotics by the model fungus Cunninghamella elegans

Khan,

Hof,

Niemcova

et al. 2024

Methods in Enzymology

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Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

Cited by 23 publications

References 62 publications

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Mycoparasites, Gut Dwellers, and Saprotrophs: Phylogenomic Reconstructions and Comparative Analyses of Kickxellomycotina Fungi

Biotransformation of fluorinated drugs and xenobiotics by the model fungus Cunninghamella elegans

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