An eight-gene molecular phylogeny of the Kickxellomycotina, including the first phylogenetic placement of Asellariales

Abstract

Kickxellomycotina is a recently described subphylum encompassing four zygomycete orders (Asellariales, Dimargaritales, Harpellales, Kickxellales). These fungi are united by the formation of disciform septal pores containing lenticular plugs. Morphological diversification and life history evolution has made the relationships within and among the four orders difficult to resolve on those grounds alone. Here we infer the phylogeny of the Kickxellomycotina based on an eight-gene supermatrix including both ribosomal rDNA (18S, 28S, 5.8S) and protein sequences (MCM7, TSR1, RPB1, RPB2, β-tubulin). The results of this study demonstrate that Kickxellomycotina is monophyletic and related to members of the Zoopagomycotina. Eight unique clades are distinguished in the Kickxellomycotina, including the four defined orders (Asellariales, Dimargaritales, Harpellales, Kickxellales) as well as four genera previously placed within two of these orders (Barbatospora, Orphella, Ramicandelaber, Spiromyces). Dimargaritales and Ramicandelaber are the earliest diverging members of the subphylum, although the relationship between these taxa remains uncertain. The remaining six clades form a monophyletic group, with Barbatospora diverging first. The next split divides the remaining members of the subphylum into two subclades: (i) Asellariales and Harpellales and (ii) Kickxellales, Orphella and Spiromyces. Estimation of ancestral states for four potentially informative morphological and ecological characters reveals that arthropod endosymbiosis might have been an important factor in the early evolution of the Kickxellomycotina.

• arthropod symbiosis
• clades
• molecular phylogenies
• mycophyletic
• zoopagomycotina

Acknowledgments

Financial support from NSF REVSYS Awards DEB-0918182 (to MMW) and DEB-0918169 (to RWL) are gratefully acknowledged for this and ongoing studies toward a molecular-based reclassification of the Kickxellomycotina. MMW received financial support for some earlier sequences in a Martin-Baker Award from the Mycological Society of America. We acknowledge the use of the Willi Hennig Society edition of TNT software. This study made use of sequences from projects from the JGI and Broad Institute, and we thank the teams involved. We thank M Berbee and J Spatafora for permission to use sequences from the Coemansia reversa genome sequencing project for our tree. We especially thank all who have contributed samples to our efforts, without which they would have never been able to proceed. In particular, we thank A Gryganskyi (and the laboratory of R Vilgalys) as well R Humber for contributing samples for many related taxa such as the Zoopagomycotina and Entomophthoromycotina. We acknowledge the particularly significant contribution to this manuscript of the work of MJ Cafaro and LG Valle on the Asellariales and Orphella, Y Degawa and Y Kurihara on Ramicandelaber and Spiromyces, and RK Benjamin on the Dimargaritales and Kickxellales. T James provided kind research support during earlier (AFTOL) training sessions to MMW and more recently. Thanks to I Robertson for significant contributions to the editing and review of this manuscript, and for overall guidance during ET’s graduate program.