Ciliates are a diverse group of microbial eukaryotes that exhibit tremendous variety in several aspects of their mating systems. To understand the evolutionary forces driving mating system diversification in ciliates, we use a comparative approach synthesizing data from many ciliate species in light of recent phylogenetic analyses. Specifically, we investigate the evolution of number of mating types, mode of mating type inheritance, and the molecular determinants of mating types across the taxonomic diversity of ciliates, with an emphasis on three well-studied genera: Tetrahymena, Paramecium, and Euplotes. We find that there have been many transitions in the number of mating types, and that the requirement of nuclear reorganization may be a more important factor than genetic exchange in determining the optimum number of mating types in a species. We also find that the molecular determinants of mating types and mode of inheritance are evolving under different constraints in different lineages of ciliates. Our results emphasize the need for further detailed examination of mating systems in understudied ciliate lineages.
Since 1999 a lineage of the pathogen Cryptococcus gattii has been infecting humans and other animals in Canada and the Pacific Northwest of the USA. It is now the largest outbreak of a life-threatening fungal infection in a healthy population in recorded history. The high virulence of outbreak strains is closely linked to the ability of the pathogen to undergo rapid mitochondrial tubularisation and proliferation following engulfment by host phagocytes. Most outbreaks spread by geographic expansion across suitable niches, but it is known that genetic re-assortment and hybridisation can also lead to rapid range and host expansion. In the context of C. gattii, however, the likelihood of virulence traits associated with the outbreak lineages spreading to other lineages via genetic exchange is currently unknown. Here we address this question by conducting outgroup crosses between distantly related C. gattii lineages (VGII and VGIII) and ingroup crosses between isolates from the same molecular type (VGII). Systematic phenotypic characterisation shows that virulence traits are transmitted to outgroups infrequently, but readily inherited during ingroup crosses. In addition, we observed higher levels of biparental (as opposed to uniparental) mitochondrial inheritance during VGII ingroup sexual mating in this species and provide evidence for mitochondrial recombination following mating. Taken together, our data suggest that hypervirulence can spread among the C. gattii lineages VGII and VGIII, potentially creating novel hypervirulent genotypes, and that current models of uniparental mitochondrial inheritance in the Cryptococcus genus may not be universal.
Cryptococcus gattii is an environmentally occurring pathogen that is responsible for causing cryptococcosis marked by pneumonia and meningoencephalitis in humans and animals. C. gattii can form long-term associations with trees and soil resulting in the production of infectious propagules (spores and desiccated yeast). The ever expanding reports of clinical and environmental isolation of C. gattii in temperate climates strongly imply C. gattii occurs world-wide. The key ability of yeast and spores to enter, survive, multiply, and exit host cells and to infect immunocompetent hosts distinguishes C. gattii as a primary pathogen and suggest evolution of C. gattii pathogenesis as a result of interaction with plants and other organisms in its environmental niche. Here we summarize the historical literature on C. gattii and recent literature supporting the world-wide occurrence of the primary pathogen C. gattii.
Unisexual reproduction is a novel homothallic sexual cycle recently discovered in both ascomycetous and basidiomycetous pathogenic fungi. It is a form of selfing that induces the yeast-to-hyphal dimorphic transition in isolates of the ␣ mating type of the human fungal pathogen Cryptococcus neoformans. Unisexual reproduction may benefit the pathogen by facilitating sexual reproduction in the absence of the opposite a mating type and by generating infectious propagules called basidiospores. Here, we report an independent potential selective advantage of unisexual reproduction beyond genetic exchange and recombination. We competed a wild-type strain capable of undergoing unisexual reproduction with mutants defective in this developmental pathway and found that unisexual reproduction provides a considerable dispersal advantage through hyphal growth and sporulation. Our results show that unisexual reproduction may serve to facilitate access to both nutrients and potential mating partners and may provide a means to maintain the capacity for dimorphic transitions in the environment. Sexual reproduction is pervasive and yet has established costs, including the time and energy devoted to locating a mate. A limited availability of mating partners of the opposite sex may further exacerbate this cost. The human fungal pathogen Cryptococcus neoformans illustrates this dilemma because its populations predominantly contain isolates of the ␣ mating type and few, if any, of the a mating type, restricting opportunities for conventional a-␣ opposite-sex mating (1, 2, 3). C. neoformans may overcome this barrier in part by undergoing unisexual reproduction-an alternative mode of sexual cycle involving cells of only one mating type, most commonly ␣ (4). Unisexual reproduction can confer benefits by generating adaptive genotypic diversity through recombination and by producing spore progeny that are readily dispersed aerially and inhaled as infectious propagules. Here, we report a novel way in which unisexual reproduction benefits C. neoformans, involving hyphal development to promote foraging and increased access to nutrients and facilitating the dispersal of spores.C. neoformans grows asexually as a budding yeast but differentiates into hyphae upon unisexual reproduction during solo culture of self-fertile isolates on appropriate growth media (4). Unisexual reproduction involves the formation of an extensive monokaryotic mycelium and terminal fruiting structures called basidia wherein meiosis occurs, and long chains of meiotic spores decorate the outer surface of the basidia (5). Components of a pheromone-responsive mitogen-activated protein kinase (MAPK) pathway are responsible for the yeast-to-hypha transition, and the absence of key elements, including the protein kinase Ste7 or the transcription factor Mat2, blocks unisexual reproduction and traps C. neoformans in the yeast form (6,7,8). While a functional MAPK pathway is necessary for morphological differentiation, the meiotic machinery, including Dmc1 and Spo11, is essential f...
Sex allocation theory has been remarkably successful at explaining the prevalence of even sex ratios in natural populations and at identifying specific conditions that can result in biased sex ratios. Much of this theory focuses on parental sex determination (SD) strategies. Here, we consider instead the evolutionary causes and consequences of mixed offspring SD strategies, in which the genotype of an individual determines not its sex, but the probability of developing one of multiple sexes. We find that alleles specifying mixed offspring SD strategies can generally outcompete alleles that specify pure strategies, but generate constraints that may prevent a population from reaching an even sex ratio. We use our model to analyze sex ratios in natural populations of Tetrahymena thermophila, a ciliate with seven sexes determined by mixed SD alleles. We show that probabilistic SD is sufficient to account for the occurrence of skewed sex ratios in natural populations of T. thermophila, provided that their effective population sizes are small. Our results highlight the importance of genetic drift in sex ratio evolution and suggest that mixed offspring SD strategies should be more common than currently thought. K E Y W O R D S :Bet hedging, biased sex ratios, frequency-dependent selection, genetic drift, mixed strategies, sex allocation, Tetrahymena thermophila.
Cryptococcus neoformans is a human-pathogenic basidiomycete that commonly infects HIV/AIDS patients to cause meningoencephalitis (7, 19). C. neoformans grows as a budding yeast during vegetative growth or as hyphae during sexual reproduction. Pseudohyphal growth of C. neoformans has been observed rarely during murine and human infections but frequently during coculture with amoeba; however, the genetics underlying pseudohyphal growth are largely unknown. Our studies found that C. neoformans displays pseudohyphal growth under nitrogen-limiting conditions, especially when a small amount of ammonium is available as a sole nitrogen source. Pseudohyphal growth was observed with Cryptococcus neoformans serotypes A and D and Cryptococcus gattii. C. neoformans pseudohyphae bud to produce yeast cells and normal smooth hemispherical colonies when transferred to complete media, indicating that pseudohyphal growth is a conditional developmental stage. Subsequent analysis revealed that two ammonium permeases encoded by the AMT1 and AMT2 genes are required for pseudohyphal growth. Both amt1 and amt2 mutants are capable of forming pseudohyphae; however, amt1 amt2 double mutants do not form pseudohyphae. Interestingly, C. gattii pseudohypha formation is irreversible and involves a RAM pathway mutation that drives pseudohyphal development. We also found that pseudohyphal growth is related to the invasive growth into the medium. These results demonstrate that pseudohyphal growth is a common reversible growth pattern in C. neoformans but a mutational genetic event in C. gattii and provide new insights into understanding pseudohyphal growth of Cryptococcus.
This study evaluated the influence of the membrane type on the performance of bioelectromethanogenesis reactors. The functional activities and taxonomic composition of bioelectrochemical systems (BES) with Nafion 117 or Ultrex CMI-7000 membranes were assessed. Functional activity was measured as methane production and current consumption rates throughout operation. Microbial biomass and phylogenetic diversity were characterized at strategic intervals related to the membrane type used. The Nafion-BES reactor showed the best performance in terms of current consumption and methane production in the early operational period and a strong selection for fermentative bacteria. However, the Nafion-BES was not able to sustain this activity over the course of 7 subpassages since methanogenic species were ultimately selected against and did not appear in the community composition for the last two subpassages. In contrast, the Ultrex-BES had a lower pH concentration gradient and lower overall current consumption activity; however, the methane production activity from the Ultrex-BES was equivalent or better than the Nafion-BES reactor and was sustained throughout the seven subpassages. The membrane type appeared to be responsible not only for differences in the electrochemical operation of the BESs but it also influenced microbial taxonomic composition and dynamics. Microbial electrosynthesis has been reported as a promising new technology for the synthesis of value-added products from CO 2 or other organic feedstocks.1 Microbial electrosynthesis relies on microbial population, applied potential, system design and the specific environmental conditions to define the final products and overall efficiencies of these systems.2-7 As a new technology, most of the studies in the area of microbial electrosynthesis address: i) proving the concept of using bacteria as electrocatalysts for targeted synthesis of a given product 8,9 and ii) understanding the mechanisms of "communication" between microbial species and electrode surfaces used as electron donors.10-13 Pure microbial cultures have primarily been used as they can provide selectivity of the synthesis process.2,12-15 However, from a practical standpoint, natural mixed microbial communities may provide a better strategy for bioelectrochemical systems exploring microbial electrosynthesis because they are more robust relative to operational changes, have greater metabolic capacity for converting/synthesizing complex substrates and are less susceptible to contamination during long-term operation. Therefore, investigations into optimal microbial communities along with interspecies interactions have also gained attention in recent years. [16][17][18][19][20][21][22][23][24][25] The practical application of microbial electrosynthesis still requires a deeper understanding of how reactor design may fundamentally impact performance and overall microbial composition. In most cases, a microbial electrosynthesis reactor is a dual-chambered system composed of an anode electrode, a cathode ele...
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