Elsevier

Mycological Research

Volume 110, Issue 12, December 2006, Pages 1379-1394
Mycological Research

A yeast clade near Candida kruisii uncovered: nine novel Candida species associated with basidioma-feeding beetles

https://doi.org/10.1016/j.mycres.2006.09.009Get rights and content

Abstract

Yeasts similar to Candida kruisii were isolated repeatedly from the digestive tracts of basidioma-feeding beetles, especially nitidulids inhabiting and feeding on a variety of agarics in the southeastern USA and Barro Colorado Island, Panama. Based on the identical sequences of the D1/D2 domains of the LSU rRNA gene (rDNA) and host beetle information, the isolates were grouped into 19 genotypes which varied from C. kruisii by up to 38 nucleotide differences in the D1/D2 region. Phylogenetic analysis of rDNA sequences and phenotypic traits placed the isolates in C. kruisii and in nine undescribed taxa. The new species and type strains are designated as Candida pallodes (NRRL Y-27653T), C. tritomae (NRRL Y-27650T), C. panamensis (NRRL Y-27657T), C. lycoperdinae (NRRL Y-27658T), C. atbi (NRRL Y-27651T), C. barrocoloradensis (NRRL Y-27934T), C. aglyptinia (NRRL Y-27935T), C. stri (NRRL Y-48063T), and C. gatunensis (NRRL Y-48064T). A phylogeny based on analysis of a combined database of sequences of SSU and LSU rDNA and the ITS region showed that the nine new species formed a novel sister clade to C. kruisii that was strongly supported by bootstrap analysis. Candida pallodes, C. tritomae, C. panamensis, and C. lycoperdinae formed one subclade, while C. atbi, C. barrocoloradensis, C. aglyptinia, C. stri, and C. gatunensis formed a second distinct subclade within the larger clade. Candida pallodes and C. atbi showed a strong host specificity to beetle species in the genus Pallodes (Coleoptera: Nitidulidae) collected from a variety of agarics. On the other hand, C. panamensis, C. tritomae, and C. lycoperdinae were associated with several unrelated beetles in Erotylidae, Scarabaeidae, Tenebrionidae, and Curculionidae as well as Lycoperdina ferruginea (Nitidulidae). Candida pallodes, C. tritomae, C. lycoperdinae, and C. atbi have been isolated repeatedly in the USA, while the other five new species have been found only at Barro Colorado Island, Panama.

Introduction

Over the last five years we examined beetles from more than twenty-five families with species tied to fungal fruiting bodies throughout their entire life history. More than 650 yeasts were isolated from the digestive tract of the basidioma-feeding beetles of which about 200 species were not known previously (Suh et al. 2005a). Although the insect-associated yeasts did not form a monophyletic group among all yeasts, many of them did form unique clades. For example, almost 30 % of all gut yeasts collected from beetles in this study were described as 16 new species (Suh et al. 2004b) in a clade with Candida tanzawaensis and a few other previously known related species (Kurtzman 2001). Other unique clades of almost exclusively insect-associated yeasts were relatives of Candida mesenterica, Candida membranifaciens, Pichia guilliermondii, and Geotrichum spp. (Suh et al., 2005b, Suh and Blackwell, 2004, Suh and Blackwell, 2005b, Suh and Blackwell, 2006). Our previous work also indicated that closely related yeasts are not necessarily associated with related hosts but with hosts sharing a habitat (e.g. Suh et al. 2005a). Strong host specificity between insects and gut yeasts, however, has been noted in some cases. For example, Candida tanzawaensis clade members, Candida choctaworum and Candida bolitotheri, have been isolated repeatedly from the tenebrionid beetles Neomida bicornis and Bolitotherus cornutus, respectively (Suh et al. 2004b). In addition to beetles, another example of close associations of yeasts with insects comes from Metschnikowia chrysoperlae and the related species, Candida picachoensis and Candida pimensis, associated only with the green lacewings, Chrysoperla spp. (Suh et al., 2004a, Nguyen et al., 2006).

During our study of beetle gut yeasts, we discovered another hidden yeast clade related to Candida kruisii. This clade includes a large number of previously unknown yeasts isolated mostly from Pallodes spp. (Coleoptera: Nitidulidae). Here we discuss the phylogenetic relationships of the yeasts and their insect-host associations and describe nine new species comprising 17 genotypes in Saccharomycotina based on DNA sequences and other taxonomic traits.

Section snippets

Yeast isolation and identification

Host beetles were collected from several localities in the southeastern USA (Louisiana, Georgia, Mississippi, Tennessee, North Carolina, and Florida) and from Barro Colorado Island, Panama (Table 1). The methods for isolating yeasts from insects were described in detail in previously published papers (Suh and Blackwell, 2004, Suh et al., 2004b). Yeast isolations also were attempted from basidiomata collected in Tennessee by dragging pieces of mushrooms with evidence of insect damage across

Taxonomy

Between 1998 and 2005, we isolated about a hundred very similar yeasts from basidioma-feeding beetles (Table 1). Except for a few isolates from beetle species in Erotylidae, Scarabaeidae, Tenebrionidae, Curculionidae, and Leiodidae, more than 80 % of the yeasts were isolated repeatedly from species of Pallodes (Nitidulidae) collected primarily in agaric basidiomata from the southeastern USA and Panama. While three isolates were cultured from the outer body surfaces or galleries of beetles, the

The Candida kruisii clade uncovered in the gut of beetles

During our study of beetle-associated yeasts, we have found that the digestive tract of beetles is an important source of novel yeasts (Suh et al., 2005a, Boekhout, 2005). About 200 apparently undescribed species have been discovered so far from the gut of basidioma-feeding beetles, and many of those yeasts form independent clades in Saccharomycotina that have not been recognized previously (Suh et al. 2005a). For example, more than 40 new beetle-associated yeast species were reported recently

Acknowledgements

We thank undergraduate students Cennet Erbil, Melissa Spera, Jonathan Lo, and Aurash Khoobehi for their very competent help in all phases of this study. We are extremely grateful for the expert identification of basidiomycetes by Clark Ovrebo and by participants of an ATBI foray in GSMNP lead by Karen Hughes and Ron Petersen and supported by their grant NSF DEB-0338699. We also appreciate the hospitality and logistical support of Hughes and Petersen. Our colleague in a joint study, Joseph V.

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