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United States Department of Agriculture

Agricultural Research Service

Research Project: FUNGAL RESOURCES FOR BIOLOGICAL CONTROL AND HIGH-VALUE USES

Location: Biological Integrated Pest Management Unit

Title: Molecular phylogeny of Entomophthoromycota

Authors
item Gryganskyi, A.P. -
item Humber, Richard
item Smith, M.E. -
item Miadlikovska, J. -
item Wu, S. -
item Voigt, K -
item Walter, G. -
item Anishchenko, I. -
item Vilgalys, R. -

Submitted to: Molecular Phylogenetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: June 22, 2012
Publication Date: August 2, 2012
Citation: Gryganskyi, A., Humber, R.A., Smith, M., Miadlikovska, J., Wu, S., Voigt, K., Walter, G., Anishchenko, I., Vilgalys, R. 2012. Molecular phylogeny of Entomophthoromycota. Molecular Phylogenetics and Evolution. 65:682-694.

Interpretive Summary: This paper presents the most comprehensive examination of gene-based relationships ever attempted for the fungi now treated in the phylum Entomophthoromycota, the most primitive group fungi that have no swimming (flagellate) spores in their life history, and one of the two largest and most important groups of fungi that are pathogens of agriculturally important insects and mite pests. These entomophthoroid fungi are extremely difficult to culture and have been the subjects of very few studies using their gene sequences. These studies have examined more than 30% of the taxa in the overall group, with samples from most of the agriculturally and medically important genera using several different approaches to molecular analyses, have calculated how long ago these fungi might have separated from all other fungi, and summarized the most probable characteristics of the ancestral fungi in this group. Grounds are laid for further molecular studies that are necessary to clarify and to revise the taxonomy of several of the genera in this group whose traditionally based taxonomy has been shown not to be supported by the molecular studies, and also to complete further studies that will completely resolve some existing controversies about the relationships of some fungi in this group to fungi in the phylum Entomophthoromycota and (as has been hypothesized in the past based on extremely limited molecular analysis) with other groups of fungi (most particularly with the fungi producing flagellate (swimming) spores. The findings reported here also represent the most extensive and detailed studies of phylogenetic (evolutionary) relationships for any group of terrestrial (nonflagellate) fungi located at the base of the fungal tree of life.

Technical Abstract: The Entomophthoromycota is a ubiquitous group of fungi best known as pathogens of a wide variety of economically important insect pests, arachnids, and other soil invertebrates, a smaller number of parasites of reptiles, vertebrates (including humans), macromycetes, fern gametophytes, and desmid algae, as well as a minority of saprobic taxa. Here we report on recent studies to resolve the phylogenetic relationships within the Entomophthoromycota and to place this group reliably among other basal fungal lineages. Bayesian Interference (BI) and Maximum Likelihood (ML) analyses of three genes (nuclear 18S and 28S rDNA, mitochondrial 16S, and the protein-coding RPB2) as well as non-molecular data consistently and unambiguously identify 31 taxa of Entomophthoromycota as a monophyletic group distinct from all other zygomycetous and flagellate fungi. Using the constraints of our multi-gene dataset we constructed the most comprehensive rDNA phylogeny yet available for Entomophthoromycota. The taxa studied here formed five distinct, well-supported lineages. The Basidiobolus clade is the earliest diverging lineage, comprised of saprobe species of Basidiobolus and the still formally undescribed snake parasite Schizangiella serpentis. The Conidiobolus lineage is represented by a paraphyletic grade of trophically diverse species that include saprobes, insect pathogens, and facultative human pathogens. Three well supported and exclusively entomopathogenic lineages in the Entomophthoraceae center around the genera Batkoa, Entomophthora and Zoophthora, although several genera within this crown clade are resolved as non-monophyletic. Ancestral state reconstruction suggests that the ancestor of all Entomophthoromycota was morphologically similar to species of Conidiobolus. Analyses using strict, relaxed, and local molecular clock models documented highly variable DNA substitution rates among lineages of Entomophthoromycota. Despite the complications caused by different rates of molecular evolution among lineages, our dating analysis indicates that the Entomophthoromycota originated 405 +/- 90 million years ago. We suggest that entomopathogenic lineages in Entomophthoraceae probably evolved from saprobic or facultatively pathogenic ancestors during or shortly after the evolutionary radiation of the insects.

Last Modified: 7/25/2014
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