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

Frances Trail,Zheng Wang,Oded Yarden,John W. Taylor,Jeffrey P. Townsend,Francesc Lopez-Giraldez,Cristina Miguel-Rojas

doi:10.1128/mbio.00192-19

Frances Trail, Zheng Wang + Show 5 more

Open Access

https://doi.org/10.1128/mbio.00192-19

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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 of Neurospora crassa germinating 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 of N. crassa colonies.IMPORTANCE One 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.

Highlights

Fungal spores germinate and undergo vegetative growth, leading to either asexual or sexual reproductive dispersal
N. crassa Conidial Germination promotes asexual development, as well as a more natural medium, i.e., maple-sap medium (MSM), which supports both asexual and sexual reproduction, we investigated the synchronous metabolic and developmental processes that occur during the germination of N. crassa conidia
Developmental differences between conidial germination on Bird medium (BM) and conidial germination of MSM were quantified, and differential regulation in gene expression was observed for genes affecting histones and genomic methylation, hyphal development, transcription factors (TFs), and responses to environmental signals

Summary

Introduction

Fungal spores germinate and undergo vegetative growth, leading to either asexual or sexual reproductive dispersal. 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. Fungi exhibit a diversity of morphology and natural history characteristics and can be found in nearly every environment inhabited by living organisms Their dispersal via spores—and, in some cases, via hyphal fragments—spawns new opportunities over long distances and creates unexpected environmental challenges for the initial growth of individual fungi [1,2,3,4]. In the typical life cycle of ascomycete fungi, vegetative growth is an adaptive mechanism functioning to maintain asexual reproduction via rapid hyphal growth and production of conidia versus reproducing sexually via production of resistant meiotic spores that survive harsh changes in the environment. In contrast, promote asexual growth, resulting in rapid dispersal

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