A closer look at Sporidiobolales: Ubiquitous microbial community members of plant and food biospheres

ABSTRACT

Carotenoid-containing yeasts in Sporidiobolales (Microbotryomycetes, Pucciniomycotina, Basidiomycota) have been reported from contrasting ecosystems, including marine, soil, phylloplane, polar ice, and many others. Here, we present several analyses drawing on 583 new isolates collected from various substrates around the globe and publicly available sequences from numerous published environmental studies. We provide a multilocus phylogenetic reconstruction of the order, estimates for total species richness, a snapshot of global distribution patterns, and analysis of niche preferences in Sporidiobolales, emphasizing their occurrence in commercial crops and food products. We evaluated loci commonly used in fungal phylogenetics, finding that RNA polymerase II subunits 1 and 2 (RPB1, RPB2) are of little utility in this group. We have reconfirmed the monophyly of Sporidiobolales with three well-supported genera, which are, in descending order of number of species, Rhodotorula, Sporobolomyces, and Rhodosporidiobolus. From our data, we estimate ca. 260 species in Sporidiobolales, of which 42 are described, and ca. 52,000 species in Pucciniomycotina. The majority of data regarding Sporidiobolales are from North America and Europe, highlighting severe knowledge gaps for most of South and Central America and Africa.

KEYWORDS:

• Basidiomycete yeasts
• biogeography
• cytochrome b
• lettuce
• Microbotryomycetes
• OTUs
• rDNA loci
• Rhodosporidium
• Sporidiobolus
• translation elongation factor 1α

ACKNOWLEDGMENTS

We thank undergraduate student Shannon Newerth and graduate student Diana Saria for helping in the isolation and molecular identification of yeast strains. We are grateful to all Aime laboratory members and colleagues who helped to enrich and/or have assisted with the maintenance of the culture collection through the years, in particular Andy Wilson, Cade Kane, Cheryl Giles, Fernando Vega, Jenni Fishburn, John Klimek, John Cavaletto, Jorge Diaz-Valderrama, Maj Padamsee, Matt Schwarzkopf, Merje Toome, Pedro Pablo Parra, Rachel Koch, Raman Kaur, Samuel Brown, Sebastian Albu, Seth Helfers, Silenze Esquivel Benjamin, Teeratas Kijpornyongpan, and Tomas Rush.

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Additional information

Funding

The work with lettuce was supported by the Center for Food Safety Engineering at Purdue University, funded by the US Department of Agriculture (USDA), Agricultural Research Service, under project 8072-42000-077-00D; travel and collecting and sequencing of the MCA collection were supported over the last decade through funding from NSF DEB 0732968 (D. Hibbett and M.C.A.), NSF DEB 1501782 (M.C.A.), NSF DEB 1556412 (M.C.A.), USDA Hatch No. 1010662 (M.C.A.), and grants from the Linnean Society of London, the Explorer’s Club, and the Louisiana Board of Regents to M.C.A.