Abstract
The Rhizopus oryzae species complex is a group of zygomycete fungi that are common, cosmopolitan saprotrophs. Some strains are used beneficially for production of Asian fermented foods but they can also act as opportunistic human pathogens. Although R. oryzae reportedly has a heterothallic (+/−) mating system, most strains have not been observed to undergo sexual reproduction and the genetic structure of its mating locus has not been characterized. Here we report on the mating behavior and genetic structure of the mating locus for 54 isolates of the R. oryzae complex. All 54 strains have a mating locus similar in overall organization to Phycomyces blakesleeanus and Mucor circinelloides (Mucoromycotina, Zygomycota). In all of these fungi, the minus (−) allele features the SexM high mobility group (HMG) gene flanked by an RNA helicase gene and a TP transporter gene (TPT). Within the R. oryzae complex, the plus (+) mating allele includes an inserted region that codes for a BTB/POZ domain gene and the SexP HMG gene. Phylogenetic analyses of multiple genes, including the mating loci (HMG, TPT, RNA helicase), ITS1-5.8S-ITS2 rDNA, RPB2, and LDH genes, identified two distinct groups of strains. These correspond to previously described sibling species R. oryzae sensu stricto and R. delemar. Within each species, discordant gene phylogenies among multiple loci suggest an outcrossing population structure. The hypothesis of random-mating is also supported by a 50∶50 ratio of plus and minus mating types in both cryptic species. When crossed with tester strains of the opposite mating type, most isolates of R. delemar failed to produce zygospores, while isolates of R. oryzae produced sterile zygospores. In spite of the reluctance of most strains to mate in vitro, the conserved sex locus structure and evidence for outcrossing suggest that a normal sexual cycle occurs in both species.
Highlights
Rhizopus oryzae is a complex of closely related, heterothallic species [1,2,3,4] that are common, cosmopolitan saprotrophs in soil, dung, and rotting vegetation [5,6,7,8]
Strains of the R. oryzae complex have been used for centuries as fermented food starters for the production of tempeh and other Asian foods [9,10,11,12,13,14] but species in this group can act as opportunistic, invasive animal and human pathogens that cause deadly infections in immuno-compromised individuals [15,16,17, 18,19,20]
Our multi-gene phylogenetic analyses support the existence of two cryptic species: R. delemar and R. oryzae
Summary
Rhizopus oryzae is a complex of closely related, heterothallic species [1,2,3,4] that are common, cosmopolitan saprotrophs in soil, dung, and rotting vegetation [5,6,7,8]. Strains of the R. oryzae complex have been used for centuries as fermented food starters for the production of tempeh and other Asian foods [9,10,11,12,13,14] but species in this group can act as opportunistic, invasive animal and human pathogens that cause deadly infections in immuno-compromised individuals [15,16,17, 18,19,20]. Compatible (+) and (2) mating types are recognizable by their mating behavior and subsequent production of meiospores (zygospores). Mating behavior is not always consistent among different strains. Zygospore germination and progeny development within the genus Rhizopus appears to be rare and has only been documented in a few cases [19,21]
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