scholarly journals Unisexual Reproduction Enhances Fungal Competitiveness by Promoting Habitat Exploration via Hyphal Growth and Sporulation

2013 ◽  
Vol 12 (8) ◽  
pp. 1155-1159 ◽  
Author(s):  
Sujal S. Phadke ◽  
Marianna Feretzaki ◽  
Joseph Heitman
Keyword(s):  
Mating Type ◽  
Wild Type Strain ◽  
Hyphal Growth ◽  
Pathogenic Fungi ◽  
Selective Advantage ◽  
Sexual Cycle ◽  
Developmental Pathway ◽  
Content Type ◽  
Human Fungal Pathogen ◽  
Unisexual Reproduction

ABSTRACT 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 α 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.

scholarly journals Identification of the Mating-Type (MAT) Locus That Controls Sexual Reproduction of Blastomyces dermatitidis

2012 ◽  
Vol 12 (1) ◽  
pp. 109-117 ◽  
Author(s):  
Wenjun Li ◽  
Thomas D. Sullivan ◽  
Eric Walton ◽  
Anna Floyd Averette ◽  
Sharadha Sakthikumar ◽  
...  
Keyword(s):  
Sexual Reproduction ◽  
Mating Type ◽  
Genetic Recombination ◽  
Sexual Cycle ◽  
Blastomyces Dermatitidis ◽  
Comparative Genomic ◽  
Dimorphic Fungi ◽  
Content Type ◽  
Long Time ◽  
Northern United States

ABSTRACTBlastomyces dermatitidisis a dimorphic fungal pathogen that primarily causes blastomycosis in the midwestern and northern United States and Canada. While the genes controlling sexual development have been known for a long time, the genes controlling sexual reproduction ofB. dermatitidis(teleomorph,Ajellomyces dermatitidis) are unknown. We identified the mating-type (MAT) locus in theB. dermatitidisgenome by comparative genomic approaches. TheB. dermatitidis MATlocus resembles those of other dimorphic fungi, containing either an alpha-box (MAT1-1) or an HMG domain (MAT1-2) gene linked to theAPN2,SLA2, andCOX13genes. However, in some strains ofB. dermatitidis, theMATlocus harbors transposable elements (TEs) that make it unusually large compared to theMATlocus of other dimorphic fungi. Based on theMATlocus sequences ofB. dermatitidis, we designed specific primers for PCR determination of the mating type. TwoB. dermatitidisisolates of opposite mating types were cocultured on mating medium. Immature sexual structures were observed starting at 3 weeks of coculture, with coiled-hyphae-containing cleistothecia developing over the next 3 to 6 weeks. Genetic recombination was detected in potential progeny by mating-type determination, PCR-restriction fragment length polymorphism (PCR-RFLP), and random amplification of polymorphic DNA (RAPD) analyses, suggesting that a meiotic sexual cycle might have been completed. The F1 progeny were sexually fertile when tested with strains of the opposite mating type. Our studies provide a model for the evolution of theMATlocus in the dimorphic and closely related fungi and open the door to classic genetic analysis and studies on the possible roles of mating and mating type in infection and virulence.

scholarly journals Genes Involved in Galactooligosaccharide Metabolism in Lactobacillus reuteri and Their Ecological Role in the Gastrointestinal Tract

2019 ◽  
Vol 85 (22) ◽  
Author(s):  
Monchaya Rattanaprasert ◽  
Jan-Peter van Pijkeren ◽  
Amanda E. Ramer-Tait ◽  
Maria Quintero ◽  
Car Reen Kok ◽  
...  
Keyword(s):  
Type Strain ◽  
Wild Type Strain ◽  
Lactobacillus Reuteri ◽  
Selective Advantage ◽  
Wild Type ◽  
Carbohydrate Source ◽  
Content Type ◽  
Gnotobiotic Mice

ABSTRACT Strains of Lactobacillus reuteri are commonly used as probiotics due to their demonstrated therapeutic properties. Many strains of L. reuteri also utilize the prebiotic galactooligosaccharide (GOS), providing a basis for formulating synergistic synbiotics that could enhance growth or persistence of this organism in vivo. In this study, in-frame deletion mutants were constructed to characterize the molecular basis of GOS utilization in L. reuteri ATCC PTA-6475. Results suggested that GOS transport relies on a permease encoded by lacS, while a second unidentified protein may function as a galactoside transporter. Two β-galactosidases, encoded by lacA and lacLM, sequentially degrade GOS oligosaccharides and GOS disaccharides, respectively. Inactivation of lacL and lacM resulted in impaired growth in the presence of GOS and lactose. In vitro competition experiments between the wild-type and ΔlacS ΔlacM strains revealed that the GOS-utilizing genes conferred a selective advantage in media with GOS but not glucose. GOS also provided an advantage to the wild-type strain in experiments in gnotobiotic mice but only on a purified, no sucrose diet. Differences in cell numbers between GOS-fed mice and mice that did not receive GOS were small, suggesting that carbohydrates other than GOS were sufficient to support growth. On a complex diet, the ΔlacS ΔlacM strain was outcompeted by the wild-type strain in gnotobiotic mice, suggesting that lacL and lacM are involved in the utilization of alternative dietary carbohydrates. Indeed, the growth of the mutants was impaired in raffinose and stachyose, which are common in plants, demonstrating that α-galactosides may constitute alternate substrates of the GOS pathway. IMPORTANCE This study shows that lac genes in Lactobacillus reuteri encode hydrolases and transporters that are necessary for the metabolism of GOS, as well as α-galactoside substrates. Coculture experiments with the wild-type strain and a gos mutant clearly demonstrated that GOS utilization confers a growth advantage in medium containing GOS as the sole carbohydrate source. However, the wild-type strain also outcompeted the mutant in germfree mice, suggesting that GOS genes in L. reuteri also provide a basis for utilization of other carbohydrates, including α-galactosides, ordinarily present in the diets of humans and other animals. Collectively, our work provides information on the metabolism of L. reuteri in its natural niche in the gut and may provide a basis for the development of synbiotic strategies.

scholarly journals Presence and Functionality of Mating Type Genes in the Supposedly Asexual Filamentous Fungus Aspergillus oryzae

2012 ◽  
Vol 78 (8) ◽  
pp. 2819-2829 ◽  
Author(s):  
Ryuta Wada ◽  
Jun-ichi Maruyama ◽  
Haruka Yamaguchi ◽  
Nanase Yamamoto ◽  
Yutaka Wagu ◽  
...  
Keyword(s):  
Gene Expression ◽  
Aspergillus Oryzae ◽  
Mating Type ◽  
Genetic Manipulation ◽  
Gene Replacement ◽  
Soy Sauce ◽  
Sexual Cycle ◽  
Dependent Manner ◽  
Content Type ◽  
Mating Type Genes

ABSTRACTThe potential for sexual reproduction inAspergillus oryzaewas assessed by investigating the presence and functionality ofMATgenes. Previous genome studies had identified aMAT1-1gene in the reference strain RIB40. We now report the existence of a complementaryMAT1-2gene and the sequencing of an idiomorphic region fromA. oryzaestrain AO6. This allowed the development of a PCR diagnostic assay, which detected isolates of theMAT1-1andMAT1-2genotypes among 180 strains assayed, including industrialtane-kojiisolates. Strains used for sake and miso production showed a near-1:1 ratio of the MAT1-1 and MAT1-2 mating types, whereas strains used for soy sauce production showed a significant bias toward the MAT1-2 mating type. MAT1-1 and MAT1-2 isogenic strains were then created by genetic manipulation of the resident idiomorph, and gene expression was compared by DNA microarray and quantitative real-time PCR (qRT-PCR) methodologies under conditions in whichMATgenes were expressed. Thirty-three genes were found to be upregulated more than 10-fold in either the MAT1-1 host strain or the MAT1-2 gene replacement strain relative to each other, showing that both theMAT1-1andMAT1-2genes functionally regulate gene expression inA. oryzaein a mating type-dependent manner, the first such report for a supposedly asexual fungus.MAT1-1expression specifically upregulated an α-pheromone precursor gene, but the functions of most of the genes affected were unknown. The results are consistent with a heterothallic breeding system inA. oryzae, and prospects for the discovery of a sexual cycle are discussed.

scholarly journals Unisexual reproduction promotes competition for mating partners in the global human fungal pathogenCryptococcus deneoformans

2019 ◽  
Author(s):  
Ci Fu ◽  
Torin P. Thielhelm ◽  
Joseph Heitman
Keyword(s):  
Mating Type ◽  
Meiotic Recombination ◽  
Species Complex ◽  
Hyphal Growth ◽  
Morphological Transition ◽  
Pheromone Response ◽  
Opposite Mating Type ◽  
Pheromone Response Pathway ◽  
Pathway Activation ◽  
Unisexual Reproduction

AbstractCourtship is pivotal for successful mating. However, courtship is challenging for theCryptococcus neoformansspecies complex, comprised of opportunistic fungal pathogens, as the majority of isolates are α mating type. In the absence of mating partners of the opposite mating type,C. deneoformanscan undergo unisexual reproduction, during which a yeast-to-hyphal morphological transition occurs. Hyphal growth during unisexual reproduction is a quantitative trait, which reflects a strain’s ability to undergo unisexual reproduction. In this study, we determined whether unisexual reproduction confers an ecological benefit by promoting foraging for mating partners. Through competitive mating assays using strains with different abilities to produce hyphae, we showed that unisexual reproduction potential did not enhance competition for mating partners of the same mating type, but when cells of the opposite mating type were present, cells with enhanced hyphal growth were more competitive for mating partners of either the same or opposite mating type. Enhanced mating competition was also observed in a strain with increased hyphal production that lacks the mating repressor geneGPA3, which contributes to the pheromone response. Hyphal growth in unisexual strains also enables contact between adjacent colonies and enhances mating efficiency during mating confrontation assays. The pheromone response pathway activation positively correlated with unisexual reproduction hyphal growth during bisexual mating and exogenous pheromone promoted bisexual cell fusion. Despite the benefit in competing for mating partners, unisexual reproduction conferred a fitness cost. Taken together, these findings suggestC. deneoformansemploys hyphal growth to facilitate contact between colonies at long distances and utilizes pheromone sensing to enhance mating competition.Author SummarySexual reproduction plays a pivotal role in shaping fungal population structure and diversity in nature. The global human fungal pathogenCryptococcus neoformansspecies complex evolved distinct sexual cycles: bisexual reproduction between mating partners of the opposite mating types, and unisexual reproduction with only one mating type. During both sexual cycles, cells undergo a yeast-to-hyphal morphological transition and nuclei diploidize through either cell-cell fusion followed by nuclear fusion during bisexual reproduction or endoreplication during unisexual reproduction. Despite the complex sexual life cycle, the majority of Cryptococcal isolates are α mating type. Albeit the scarcity ofMATacells in the environment, meiotic recombination is prevalent. To decipher this conundrum, we ask whether there is an underlying mechanism in whichCryptococcusspecies increase their mating opportunities. In this study, we showed that the undirected hyphal growth during unisexual reproduction enablesMATα cells to forage for mating partners over a larger surface area, and whenMATα hyphae come into close proximity of rareMATacells, pheromone response pathway activation in bothMATα andMATacells can further enhance mating. This mating enhancement could promote outcrossing and facilitate genome reshuffling via meiotic recombination.

scholarly journals A Novel Nitrogen and Carbon Metabolism Regulatory Cascade Is Implicated in Entomopathogenicity of the Fungus Metarhizium robertsii

mSystems ◽  
2021 ◽  
Author(s):  
Yamin Meng ◽  
Xing Zhang ◽  
Dan Tang ◽  
Xiaoxuan Chen ◽  
Dan Zhang ◽  
...  
Keyword(s):  
Carbon Metabolism ◽  
Hyphal Growth ◽  
Pathogenic Fungi ◽  
Mitogen Activated Protein Kinase ◽  
Physical Barrier ◽  
Metarhizium Robertsii ◽  
Content Type ◽  
Regulatory Cascade ◽  
Mitogen Activated Protein ◽  
Nutrient Selection

Penetration of the cuticle, the first physical barrier to pathogenic fungi, is the prerequisite for fungal infection of insects. In the entomopathogenic fungus Metarhizium robertsii , we found that the Fus3–mitogen-activated protein kinase (MAPK) and the transcription factor regulator of nutrient selection 1 (RNS1) constitute a novel cascade that controls cuticle penetration by regulating degradation of cuticular lipids, proteins, and chitin to obtain nutrients for hyphal growth and entry into the insect hemocoel.

scholarly journals Multiple Pathways to Homothallism in Closely Related Yeast Lineages in the Basidiomycota

mBio ◽  
2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Alexandra Cabrita ◽  
Márcia David-Palma ◽  
Patrícia H. Brito ◽  
Joseph Heitman ◽  
Marco A. Coelho ◽  
...  
Keyword(s):  
Sexual Reproduction ◽  
Mating Type ◽  
Protein Interactions ◽  
Single Species ◽  
Phaffia Rhodozyma ◽  
Sexual Cycle ◽  
Natural Setting ◽  
Single Individual ◽  
Content Type ◽  
Heterothallic Species

ABSTRACT Sexual reproduction in fungi relies on proteins with well-known functions encoded by the mating type (MAT) loci. In the Basidiomycota, MAT loci are often bipartite, with the P/R locus encoding pheromone precursors and pheromone receptors and the HD locus encoding heterodimerizing homeodomain transcription factors (Hd1/Hd2). The interplay between different alleles of these genes within a single species usually generates at least two compatible mating types. However, a minority of species are homothallic, reproducing sexually without an obligate need for a compatible partner. Here, we examine the organization and function of the MAT loci of Cystofilobasidium capitatum, a species in the order Cystofilobasidiales, which is unusually rich in homothallic species. We determined MAT gene content and organization in C. capitatum and found that it resembles a mating type of the closely related heterothallic species Cystofilobasidium ferigula. To explain the homothallic sexual reproduction observed in C. capitatum, we examined HD protein interactions in the two Cystofilobasidium species and determined C. capitatum MAT gene expression both in a natural setting and upon heterologous expression in Phaffia rhodozyma, a homothallic species belonging to a clade sister to that of Cystofilobasidium. We conclude that the molecular basis for homothallism in C. capitatum appears to be distinct from that previously established for P. rhodozyma. Unlike in the latter species, homothallism in C. capitatum may involve constitutive activation or dispensability of the pheromone receptor and the functional replacement of the usual Hd1/Hd2 heterodimer by an Hd2 homodimer. Overall, our results suggest that homothallism evolved multiple times within the Cystofilobasidiales. IMPORTANCE Sexual reproduction is important for the biology of eukaryotes because it strongly impacts the dynamics of genetic variation. In fungi, although sexual reproduction is usually associated with the fusion between cells belonging to different individuals (heterothallism), sometimes a single individual is capable of completing the sexual cycle alone (homothallism). Homothallic species are unusually common in a fungal lineage named Cystofilobasidiales. Here, we studied the genetic bases of homothallism in one species in this lineage, Cystofilobasidium capitatum, and found it to be different in several aspects from those of another homothallic species, Phaffia rhodozyma, belonging to the genus most closely related to Cystofilobasidium. Our results strongly suggest that homothallism evolved independently in Phaffia and Cystofilobasidium, lending support to the idea that transitions between heterothallism and homothallism are not as infrequent as previously thought. Our work also helps to establish the Cystofilobasidiales as a model lineage in which to study these transitions.

scholarly journals N-Acetylglucosamine Induces White-to-Opaque Switching and Mating in Candida tropicalis, Providing New Insights into Adaptation and Fungal Sexual Evolution

2012 ◽  
Vol 11 (6) ◽  
pp. 773-782 ◽  
Author(s):  
Jing Xie ◽  
Han Du ◽  
Guobo Guan ◽  
Yaojun Tong ◽  
Themistoklis K. Kourkoumpetis ◽  
...  
Keyword(s):  
Candida Tropicalis ◽  
Fungal Pathogen ◽  
Intermediate Phase ◽  
Cell Formation ◽  
Pathogenic Fungi ◽  
Opportunistic Pathogen ◽  
Phenotypic Switching ◽  
Content Type ◽  
Human Fungal Pathogen ◽  
Sexual Mating

ABSTRACTPathogenic fungi are capable of switching between different phenotypes, each of which has a different biological advantage. In the most prevalent human fungal pathogen,Candida albicans, phenotypic transitions not only improve its adaptation to a continuously changing host microenvironment but also regulate sexual mating. In this report, we show thatCandida tropicalis, another important human opportunistic pathogen, undergoes reversible and heritable phenotypic switching, referred to as the “white-opaque” transition. Here we show thatN-acetylglucosamine (GlcNAc), an inducer of white-to-opaque switching inC. albicans, promotes opaque-cell formation and mating and also inhibits filamentation in a number of naturalC. tropicalisstrains. Our results suggest that host chemical signals may facilitate this phenotypic switching and mating ofC. tropicalis, which had been previously thought to reproduce asexually. Overexpression of theC. tropicalis WOR1gene inC. albicansinduces opaque-cell formation. Additionally, an intermediate phase between white and opaque was observed inC. tropicalis, indicating that the switching could be tristable.

scholarly journals Uniparental sexual reproduction following cell-cell fusion of opposite mating-type partners

2020 ◽  
Author(s):  
Vikas Yadav ◽  
Sheng Sun ◽  
Joseph Heitman
Keyword(s):  
Mating Type ◽  
Genetic Material ◽  
Nuclear Genome ◽  
Sexual Cycle ◽  
Uniparental Inheritance ◽  
Opposite Mating Type ◽  
Fluorescent Reporter ◽  
Unisexual Reproduction ◽  
F1 Progeny ◽  
Opposite Sex

AbstractSome animal species require an opposite-sex partner for their sexual development but discard the partner’s genome before gamete formation, generating hemi-clonal progeny in a process called hybridogenesis. In this study, we discovered hybridogenesis-like reproduction in a basidiomycete fungus, Cryptococcus neoformans. C. neoformans has two mating types, MATa and MATα, which fuse to produce a dikaryotic zygote that completes a sexual cycle producing recombinant meiotic progeny. Here, we discovered exclusive uniparental inheritance of nuclear genetic material in a fraction of the F1 progeny produced during bisexual reproduction of two opposite mating-type partners. By analyzing strains expressing fluorescent reporter proteins, we observed that dikaryotic hyphae were produced, but only one parental nuclei was found in the terminal basidium where sporulation occurs. Whole-genome sequencing revealed the nuclear genome of the progeny was identical with one or the other parental genome, whereas the mitochondrial genome was always inherited from the MATa parent. Uniparental sporulation was also observed in natural isolate crosses occurring in concert with biparental sporulation. The meiotic recombinase Dmc1 was found to be critical for uniparental reproduction. These findings reveal an unusual mode of eukaryotic microbial unisexual reproduction that shares features with hybridogenesis in animals.

scholarly journals Comparative Evolution of Morphological Regulatory Functions in Candida Species

2013 ◽  
Vol 12 (10) ◽  
pp. 1356-1368 ◽  
Author(s):  
Erika Lackey ◽  
Geethanjali Vipulanandan ◽  
Delma S. Childers ◽  
David Kadosh
Keyword(s):  
Target Genes ◽  
Pathogenic Fungi ◽  
Specific Gene ◽  
Content Type ◽  
Environmental Signals ◽  
Human Fungal Pathogen ◽  
Evolutionarily Conserved ◽  
Morphological Transitions ◽  
High Level ◽  
Regulatory Functions

ABSTRACTMorphological transitions play an important role in virulence and virulence-related processes in a wide variety of pathogenic fungi, including the most commonly isolated human fungal pathogenCandida albicans. While environmental signals, transcriptional regulators, and target genes associated withC. albicansmorphogenesis are well-characterized, considerably little is known about morphological regulatory mechanisms and the extent to which they are evolutionarily conserved in less pathogenic and less filamentous non-albicans Candidaspecies (NACS). We have identified specific optimal filament-inducing conditions for three NACS (C. tropicalis,C. parapsilosis, andC. guilliermondii), which are very limited, suggesting that these species may be adapted for niche-specific filamentation in the host. Only a subset of evolutionarily conservedC. albicansfilament-specific target genes were induced upon filamentation inC. tropicalis,C. parapsilosis, andC. guilliermondii. One of the genes showing conserved expression wasUME6, a key filament-specific regulator ofC. albicanshyphal development. Constitutive high-level expression ofUME6was sufficient to drive increased filamentation as well as biofilm formation and partly restore conserved filament-specific gene expression in bothC. tropicalisandC. parapsilosis, suggesting that evolutionary differences in filamentation ability among pathogenicCandidaspecies may be partially attributed to alterations in the expression level of a conserved filamentous growth machinery. In contrast toUME6,NRG1, an important repressor ofC. albicansfilamentation, showed only a partly conserved role in controlling NACS filamentation. Overall, our results suggest thatC. albicansmorphological regulatory functions are partially conserved in NACS and have evolved to respond to more specific sets of host environmental cues.

scholarly journals Pseudohyphal Regulation by the Transcription Factor Rfg1p in Candida albicans

2010 ◽  
Vol 9 (9) ◽  
pp. 1363-1373 ◽  
Author(s):  
Ian A. Cleary ◽  
Priyadarshini Mulabagal ◽  
Sara M. Reinhard ◽  
Nishant P. Yadev ◽  
Craig Murdoch ◽  
...  
Keyword(s):  
Candida Albicans ◽  
Hyphal Growth ◽  
Growth Conditions ◽  
Pcr Analysis ◽  
Yeast Growth ◽  
Content Type ◽  
Human Fungal Pathogen ◽  
Hypha Formation

ABSTRACT The opportunistic human fungal pathogen Candida albicans is a major cause of nosocomial infections. One of the fundamental features of C. albicans pathogenesis is the yeast-to-hypha transition. Hypha formation is controlled positively by transcription factors such as Efg1p and Cph1p, which are required for hyphal growth, and negatively by Tup1p, Rfg1p, and Nrg1p. Previous work by our group has shown that modulating NRG1 gene expression, hence altering morphology, is intimately linked to the capacity of C. albicans to cause disease. To further dissect these virulence mechanisms, we employed the same strategy to analyze the role of Rfg1p in filamentation and virulence. Studies using a tet-RFG1 strain revealed that RFG1 overexpression does not inhibit hypha formation in vitro or in the mouse model of hematogenously disseminated candidiasis. Interestingly, RFG1 overexpression drives formation of pseudohyphae under yeast growth conditions—a phenotype similar to that of C. albicans strains with mutations in one of several mitotic regulatory genes. Complementation assays and real-time PCR analysis indicate that, although the morphology of the tet-RFG1 strain resembles that of the mitotic regulator mutants, Rfg1p overexpression does not impact expression of these genes.

Sign in / Sign up

Export Citation Format

Share Document