Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts

doi:10.1371/journal.ppat.1009656

	Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts
	Mei, Lijuan 1,2; Wang, Xuewen 1,2; Yin, Ying 1; Tang, Guirong 1; Wang, Chengshu1,2,3
	2021-06
发表期刊	PLOS PATHOGENS (IF:5.5[JCR-2023],5.5[5-Year])
ISSN	1553-7366
EISSN	1553-7374
卷号	17 期号:6
DOI	10.1371/journal.ppat.1009656
摘要	The exopolysaccharide galactosaminogalactan (GAG) has been well characterized in Aspergilli, especially the human pathogen Aspergillus fumigatus. It has been found that a five-gene cluster is responsible for GAG biosynthesis in Aspergilli to mediate fungal adherence, biofilm formation, immunosuppression or induction of host immune defences. Herein, we report the presence of the conserved GAG biosynthetic gene cluster in the insect pathogenic fungus Metarhizium robertsii to mediate either similar or unique biological functions. Deletion of the gene cluster disabled fungal ability to produce GAG on germ tubes, mycelia and appressoria. Relative to the wild type strain, null mutant was impaired in topical infection but not injection of insect hosts. We found that GAG production by Metarhizium is partially acetylated and could mediate fungal adherence to hydrophobic insect cuticles, biofilm formation, and penetration of insect cuticles. In particular, it was first confirmed that this exopolymer is responsible for the formation of appressorium mucilage, the essential extracellular matrix formed along with the infection structure differentiation to mediate cell attachment and expression of cuticle degrading enzymes. In contrast to its production during A. fumigatus invasive growth, GAG is not produced on the Metarhizium cells harvested from insect hemocoels; however, the polymer can glue germ tubes into aggregates to form mycelium pellets in liquid culture. The results of this study unravel the biosynthesis and unique function of GAG in a fungal system apart from the aspergilli species. Author summary Fungal cell wall associated exopolymer GAG was first identified from Aspergillus niger decades ago and has been well characterized in terms of its biosynthetic mechanism, pathological and biological functions in Aspergillus fungi, especially the human pathogen A. fumigatus. With the accomplishment of diverse fungal genomes, the conserved GAG biosynthetic gene cluster is found to patchily distribute in fungal species beyond Aspergilli. However, until this study, the contribution of the clustered genes to GAG production has not been investigated in any non-Aspergillus fungi. We performed gene deletions and functional characterizations of GAG in an insect pathogenic fungus Metarhizium robertsii, and found that the partially acetylated GAG can be produced by the fungus to contribute to fungal virulence during topical infection of insect hosts. This exopolymer can be produced on germ tubes, mycelia and appressoria to mediate cell adherence, cuticle penetration, biofilm formation, mycelium aggregation in liquid culture and in particular, appressorium mucilaginous matrix formation. In addition, it was found that loss of GAG production could alter appressorium protein expressions including the enzymes involved in degrading insect cuticles. Our data advance the understanding of GAG biosynthesis and functions in an animal pathogenic fungus that is highly divergent from Aspergilli.
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收录类别	SCIE
语种	英语
WOS研究方向	Microbiology ; Parasitology ; Virology
WOS类目	Microbiology ; Parasitology ; Virology
WOS记录号	WOS:000664723300002
出版者	PUBLIC LIBRARY SCIENCE
原始文献类型	Article
引用统计	正在获取...
文献类型	期刊论文
条目标识符	https://kms.shanghaitech.edu.cn/handle/2MSLDSTB/127613
专题	生命科学与技术学院_特聘教授组_王成树组
通讯作者	Wang, Chengshu
作者单位	1.Chinese Acad Sci, Shanghai Inst Plant Physiol & Ecol, CAS Ctr Excellence Mol Plant Sci, CAS Key Lab Insect Dev & Evolutionary Biol, Shanghai, Peoples R China; 2.Chinese Acad Sci, CAS Ctr Excellence Biot Interact, Beijing, Peoples R China; 3.ShanghaiTech Univ, Sch Life Sci & Technol, Shanghai, Peoples R China
通讯作者单位	生命科学与技术学院
推荐引用方式 GB/T 7714	Mei, Lijuan,Wang, Xuewen,Yin, Ying,et al. Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts[J]. PLOS PATHOGENS,2021,17(6).
APA	Mei, Lijuan,Wang, Xuewen,Yin, Ying,Tang, Guirong,&Wang, Chengshu.(2021).Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts.PLOS PATHOGENS,17(6).
MLA	Mei, Lijuan,et al."Conservative production of galactosaminogalactan in Metarhizium is responsible for appressorium mucilage production and topical infection of insect hosts".PLOS PATHOGENS 17.6(2021).