Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>

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 met...

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Autores principales:	Zheng Wang, Cristina Miguel-Rojas, Francesc Lopez-Giraldez, Oded Yarden, Frances Trail, Jeffrey P. Townsend
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	artificial medium asexual development asexual-sexual switch conidiospore filamentous fungi germination Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/bef046e5b3394990941e66886702e300
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spelling	oai:doaj.org-article:bef046e5b3394990941e66886702e3002021-11-15T15:55:25ZMetabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>10.1128/mBio.00192-192150-7511https://doaj.org/article/bef046e5b3394990941e66886702e3002019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00192-19https://doaj.org/toc/2150-7511ABSTRACT 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.Zheng WangCristina Miguel-RojasFrancesc Lopez-GiraldezOded YardenFrances TrailJeffrey P. TownsendAmerican Society for Microbiologyarticleartificial mediumasexual developmentasexual-sexual switchconidiosporefilamentous fungigerminationMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	artificial medium asexual development asexual-sexual switch conidiospore filamentous fungi germination Microbiology QR1-502
spellingShingle	artificial medium asexual development asexual-sexual switch conidiospore filamentous fungi germination Microbiology QR1-502 Zheng Wang Cristina Miguel-Rojas Francesc Lopez-Giraldez Oded Yarden Frances Trail Jeffrey P. Townsend Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
description	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.
format	article
author	Zheng Wang Cristina Miguel-Rojas Francesc Lopez-Giraldez Oded Yarden Frances Trail Jeffrey P. Townsend
author_facet	Zheng Wang Cristina Miguel-Rojas Francesc Lopez-Giraldez Oded Yarden Frances Trail Jeffrey P. Townsend
author_sort	Zheng Wang
title	Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
title_short	Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
title_full	Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
title_fullStr	Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
title_full_unstemmed	Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>
title_sort	metabolism and development during conidial germination in response to a carbon-nitrogen-rich synthetic or a natural source of nutrition in <italic toggle="yes">neurospora crassa</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/bef046e5b3394990941e66886702e300
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Metabolism and Development during Conidial Germination in Response to a Carbon-Nitrogen-Rich Synthetic or a Natural Source of Nutrition in <italic toggle="yes">Neurospora crassa</italic>

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