Diverse Heat Tolerance of the Yeast Symbionts of Platycerus Stag Beetles in Japan.

Xue-Jiao Zhu,Sheng-Nan Zhang,Noriko Kubota,Masahiko Tanahashi,Kako Kawakami,Kana Watanabe,Xiu-Jun Wen,Kôhei Kubota,Etsuro Takagi

doi:10.3389/fmicb.2021.793592

Abstract

The genus Platycerus (Coleoptera: Lucanidae) is a small stag beetle group, which is adapted to cool-temperate deciduous broad-leaved forests in East Asia. Ten Platycerus species in Japan form a monophyletic clade endemic to Japan and inhabit species-specific climatic zones. They are reported to have co-evolutionary associations with their yeast symbionts of the genus Sheffersomyces based on host cytochrome oxidase subunit I (COI) and yeast intergenic spacer (IGS) phylogenies. Here we examined the heat tolerances of the yeast colonies isolated from the mycangia of 37 females belonging ten Japanese Platycerus species. The upper limits of growth and survival temperatures of each colony were decided by cultivating it at ten temperature levels between 17.5 and 40°C. Although both temperatures varied during 25.0–31.25°C, the maximum survival temperatures (MSTs) were a little higher than the maximum growth temperatures (MGTs) in 16 colonies. Pearson’s correlations between these temperatures and environmental factors (elevation and 19 bioclimatic variables from Worldclim database) of host beetle collection sites were calculated. These temperatures were significantly correlated with elevation negatively, the maximum temperature of the warmest month (Bio5) positively, and some precipitative variables, especially in the warm season (Bio12, 13, 16, 18) negatively. Sympatric Platycerus kawadai and Platycerus albisomni share the same lineage of yeast symbionts that exhibit the same heat tolerance, but the elevational lower range limit of P. kawadai is higher than that of P. albisomni. Based on the field survey in their sympatric site, the maximum temperature of host wood of P. kawadai larvae is higher about 2–3°C than that of P. albisomni larvae in the summer, which may restrict the elevational range of P. kawadai to higher area. In conclusion, it is suggested that the heat tolerance of yeast symbionts restricts the habitat range of their host Platycerus species or/and that the environmental condition that host Platycerus species prefers affect the heat tolerance of its yeast symbionts.

Highlights

Diverse insect taxa and fungi can have mutualistic relationships (Biedermann and Vega, 2020)
The maximum growth temperatures (MGTs) and maximum survival temperatures (MSTs) of the yeast symbionts of each Platycerus species ranged between 25.0 and 31.25◦C, and the MST was higher than the MGT in 16 strains
Symbionts of the sugitai species group (Platycerus akitaorum, Platycerus sugitai, and Platycerus urushiyamai) and P. sue (Clade Ic according to intergenic spacer (IGS) based phylogeny; Table 1 and Figure 2) were relatively vulnerable to high temperatures (MGT: 25.0–27.25◦C; MST: 25.0–27.5◦C)

Summary

Introduction

Diverse insect taxa and fungi can have mutualistic relationships (Biedermann and Vega, 2020). Symbiotic relationships with fungi are especially critical for wood-feeding insects, because wood consists of polymers that are indigestible to insects such as cellulose, hemicellulose, and lignin (Haack and Slansky, 1987; Geib et al, 2008; Stokland, 2012). Female stag beetles (family Lucanidae) possess mycangia in the form of an exoskeletal organ on the dorsal side of the abdominal tip that carries microbial symbionts (Tanahashi et al, 2010; Tanahashi and Hawes, 2016; Kubota et al, 2020). Stag beetles mainly feed on decaying wood (Tanahashi and Kubota, 2013; Tanahashi et al, 2018) and commonly carry yeast symbionts belonging to the genus Scheffersomyces, a xylosefermenting group of yeasts (Du Preez and Prior, 1985; Jeffries and Kurtzman, 1994; Olsson and Hahn-Hägerdal, 1996). Xylose is the main component of hemicellulose in broad-leaved tree species (Sjöström, 1993)

Methods

Results

Conclusion