A new genus Unguispora in Kickxellales shows an intermediate lifestyle between saprobic and gut-inhabiting fungi

ABSTRACT

Kickxellomycotina encompasses two fungal groups: a saprobic group in excrement and soil and an arthropod gut-inhabiting group. The evolutionary transition between these two lifestyles is unclear due to the lack of knowledge on intermediate forms and lifestyles. Here, we describe a new species, Unguispora rhaphidophoridarum, that was isolated from the excrement of cave crickets (Rhaphidophoridae) in Japan. This species has a novel lifestyle that is intermediate between the saprobic and gut-inhabiting groups. The new genus Unguispora is a member of the Kickxellales and characterized by the sterile appendages born on the sporocladium and by the claw-like ornamentation of the sporangiole. Phylogenetic analysis based on 18S and 28S nuclear ribosomal DNA showed that this fungus is distinct from all known kickxellalean genera and is sister to Linderina. The sporangiospore of the new species germinated only in anaerobiosis and grew in a yeast-like form. The yeast-like cells, defined as “secondary spores,” germinated into hyphae in aerobiosis. In the alimentary tract of cave crickets, the sporangiola are attached to the proventriculus (foregut) by the claw-like ornamentation and multiplicate in the same yeast-like form as under culture. We introduce a new term, “amphibious fungi,” to describe fungi that have two life stages, one outside and the other inside the host gut, like U. rhaphidophoridarum. The discovery of an amphibious fungus in Kickxellales, which was formerly considered to be only saprobic, suggests that Kickxellomycotina has evolved in association with the animal gut.

KEYWORDS:

• Cave crickets
• Kickxellomycotina
• morphological transition
• SEM
• Zoopagomycota
• 2 new taxa

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ACKNOWLEDGMENTS

We thank Ryuichiro Machida for providing his knowledge of insects to us and Hiroshi Masumoto for general help and useful discussion.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by JSPS KAKENHI grants JP2529108 (2013–2015) (to Y.D.) and JP19H03281 (2019–2022) (to Y.D.), “Innovation inspired by Nature” Research Support Program, Sekisui Chemical Co., Ltd., in 2013 (to Y.D.), general research grant from the Institute for Fermentation, Osaka (G-2019-1-098 [2019]) (to Y.D.), and the fund of Nagano Prefecture to promote scientific activity (2020) (to T.R.).