Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in Neurospora crassa

Abstract

Fungal spores germinate and undergo vegetative growth, leading to either asexual or sexual reproductive dispersal. Previous research has indicated that among developmental regulatory genes, expression is conserved across nutritional environments, whereas pathways for carbon and nitrogen metabolism appear highly responsive—perhaps to accommodate differential nutritive processing. To comprehensively investigate conidial germination and the adaptive life history decision-making underlying these two modes of reproduction, we profiled transcription ofNeurospora crassagerminating on two media: synthetic Bird medium, designed to promote asexual reproduction; and a natural maple sap medium, on which both asexual reproduction and sexual reproduction manifest. A later start to germination but faster development was observed on synthetic medium. Metabolic genes exhibited altered expression in response to nutrients—at least 34% of the genes in the genome were significantly downregulated during the first two stages of conidial germination on synthetic medium. Knockouts of genes exhibiting differential expression across development altered germination and growth rates, as well as in one case causing abnormal germination. A consensus Bayesian network of these genes indicated especially tight integration of environmental sensing, asexual and sexual development, and nitrogen metabolism on a natural medium, suggesting that in natural environments, a more dynamic and tentative balance of asexual and sexual development may be typical ofN. crassacolonies.IMPORTANCEOne of the most remarkable successes of life is its ability to flourish in response to temporally and spatially varying environments. Fungi occupy diverse ecosystems, and their sensitivity to these environmental changes often drives major fungal life history decisions, including the major switch from vegetative growth to asexual or sexual reproduction. Spore germination comprises the first and simplest stage of vegetative growth. We examined the dependence of this early life history on the nutritional environment using genome-wide transcriptomics. We demonstrated that for developmental regulatory genes, expression was generally conserved across nutritional environments, whereas metabolic gene expression was highly labile. The level of activation of developmental genes did depend on current nutrient conditions, as did the modularity of metabolic and developmental response network interactions. This knowledge is critical to the development of future technologies that could manipulate fungal growth for medical, agricultural, or industrial purposes.

Integrative Activity of Mating Loci, Environmentally Responsive Genes, and Secondary Metabolism Pathways during Sexual Development of Chaetomium globosum

“…Our previous studies demonstrated that genes inferred to play central roles in the network model tend to be placed in the top-tier modules and have multiple edge connections (6, 64)—consistent with a conception that gene hubs in the network represent critical points (82, 83). Bayesian networks (BN) were constructed in this study to examine interactions of selected conidiation, het , and sexual development regulatory genes during perithecial development, including ascus development protein coding gene ( asd ) (Fig.…”

“…The degrees of expression of these HKs were divergent during N. crassa conidium germination between different media (64). All these HKs exhibited similar patterns of downregulation when N.…”

“…To investigate how differences in regulation of expression might contribute to divergence in development and ecology among closely related species, we conducted comparative transcriptomic sequencing of Chaetomium globosum, Neurospora spp. (5, 6, 64), and Fusarium spp. (7, 56).…”

Marked Neurospora crassa Strains for Competition Experiments and Bayesian Methods for Fitness Estimates

“…In a facultative sexual species such as N. crassa both mating types have to be maintained in a population for sexual reproduction to occur; so it seems unexpected that one mating type has a higher asexual fitness than the other. However, it has been reported previously that in N. crassa mat a has a higher growth rate than mat A (Ryan et al 1943), and that germination of mat A conidia is slightly slower (Wang et al 2019). This difference can be understood in the light of gene expression differences, as many genes unrelated to sexual reproduction are expressed differently in the vegetative mycelium of the different mating types, despite that these lines are nearly isogenic except for the mating type locus (Wang et al 2012).…”

Sporulation environment drives phenotypic variation in the pathogenAspergillus fumigatus

“…Breaking dormancy, or germinating, is arguably the most important step in pathogenesis for these fungi. Historically studies have focused on the germination environment, addressing factors such as temperature, inoculum density, carbon source, nitrogen source, and pH 4-8 . However, despite the wide range of environments in which fungal spores are produced and their importance as disease agents, the impact of sporulation environment on germination has been largely ignored.…”