Kwoniella mangroviensisgen. nov., sp. nov. (Tremellales,Basidiomycota), a teleomorphic yeast from mangrove habitats in the Florida Everglades and Bahamas

Abstract

Mangrove forests inhabit the shoreline regions of tropical and subtropical marine habitats, where they are the basis of a multi-trophic level food web that drives the shellfish and fisheries industries. Yeasts, and other fungi, have significant roles in these ecosystems as they decompose plant organic material and serve as a food source for small invertebrates. Studies designed to examine yeast communities of mangrove regions of the Florida Everglades and the Bahamas demonstrated the repeated presence of an undescribed teleomorphic basidiomycetous yeast. The yeast is heterothallic, with a sexual cycle that can be observed on artificial media. Mating between compatible pairs produces polymorphic basidia. Some basidia are globose, ovoid or lageniform, with longitudinal to oblique and transverse septa, whereas other basidia are navicular with one to three transverse septa. Basidiocarps and ballistoconidia are absent. Molecular sequence analysis of a partial region (D1/D2 domains) of the large subunit rRNA demonstrated that the yeast is phylogenetically distinct from other teleomorphic Tremellales with close relationships to the anamorphic species Cryptococcus dejecticola, Cryptococcus bestiolae and Bullera dendrophila. The molecular and phenotypic data indicate that this teleomorph should be classified in a novel genus. Therefore, Kwoniella mangroviensis gen. nov., sp. nov. (Type strain CBS 8507), is proposed.

Molecular and Genetic Evidence for a Tetrapolar Mating System in the Basidiomycetous Yeast Kwoniella mangrovensis and Two Novel Sibling Species

“…They also determined LSU and ITS sequences for representative strains and found little genetic variability, except for one cork isolate and the beach isolate, which had one nucleotide substitution in LSU and 6 to 7 substitutions in ITS, compared to the mangrove strains. These differences were not considered sufficient by Statzell-Tallman et al (13) to warrant separate taxonomic status for those strains without further mating and genetic studies.…”

“…In the present study, we have complemented the MLST approach with the analysis of MAT genes due to the central role played by MAT loci in regulating sexual reproduction and thus in determining species boundaries (1,3). The multilocus approach involved five K. mangrovensis strains (four from seawater and one from cork) from the original study (13), as well as one additional isolate from the British Virgin Islands, one clinical isolate from the United States, four isolates from Mopane trees in Botswana, one isolate from a tree hollow in Brazil, and two isolates from grapes in Europe (see Table S1 in the supplemental material). The results showed that the tropical seawater isolates, which included the type strain of K. mangrovensis, formed a monophyletic lineage, while the four Botswana isolates and the three European strains formed two additional sister lineages ( Fig.…”

“…A multilocus sequence typing (MLST) approach was applied to a set of 14 strains previously identified as K. mangrovensis on the basis of the sequences of the D1/D2 domains of the LSU rRNA gene (LSU). The set of strains comprised five strains included in the original study of Statzell-Tallman et al (13), four seawater isolates from the Bahamas (K01, K02, K04, K06) and one cork isolate (CECT 11955 ϭ K25), and nine additional strains: one clinical isolate from the United States (K09), four isolates from Mopane trees in Botswana, one seawater isolate from the British Virgin Islands (CBS 11279 ϭ K27), one isolate from grape juice in Switzerland (CBS 7868 ϭ K28), one isolate from grape berries in Slovenia (ZIM 605 ϭ K29) obtained by Č adež et al (29), and one isolate from a tree hollow in Brazil (K30) (see Table S1 in the supplemental material). The isolates from the Florida Everglades and the beach isolate reported by Statzell-Tallman et al (13) were no longer viable (J. W. Fell, personal communication) and could thus not be studied.…”

“…In view of the results of previous studies that explored the MAT locus structure in those yeasts, it seemed essential to examine this genomic region in strains from the original description of K. mangrovensis to verify its mating system and to seek additional insights on the evolution of MAT in the Tremellales. Statzell-Tallman et al (13) included in their study two cork isolates from Europe which had divergent internal transcribed spacer (ITS) sequences but were considered conspecific with the mangrove strains. We expanded our study to include additional isolates from different substrates and geographic locations, identified as K. mangrovensis on the basis of large subunit (LSU) rRNA gene sequences, and applied a multilocus sequencing approach to reassess species limits and disclose putative cryptic species.…”

“…Kwoniella mangrovensis (the original spelling, mangroviensis, was considered an orthographical error) was described as a sexual species with a bipolar mating system based on the study of several isolates from mangrove habitats in the Bahamas and Florida Everglades (13). On the basis of phylogenetic analysis of multiple genes (14), this species belongs, together with Kwoniella (Cryptococcus) heveanensis, to the Kwoniella clade, a sister clade to that which contains the pathogenic Cryptococcus neoformans and Cryptococcus gattii, as well as C. amylolentus (Filobasidiella clade, which we henceforth rename as the Cryptococcus clade for reasons that will be explained in Discussion).…”