Fungal commensalism modulated by a dual-action phosphate transceptor

Yuanyuan Wang; Jia Zhou; Yun Zou; Xiaoqing Chen; Lin Liu; Wanjun Qi; Xinhua Huang; Changbin Chen; Ning-Ning Liu

doi:10.1016/j.celrep.2021.110293

Fungal commensalism modulated by a dual-action phosphate transceptor

Cell Rep. 2022 Jan 25;38(4):110293. doi: 10.1016/j.celrep.2021.110293.

Authors

Yuanyuan Wang¹, Jia Zhou², Yun Zou¹, Xiaoqing Chen³, Lin Liu², Wanjun Qi⁴, Xinhua Huang⁵, Changbin Chen⁶, Ning-Ning Liu⁷

Affiliations

¹ The Center for Microbes, Development, and Health, Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China; The University of Chinese Academy of Sciences, Beijing, China; The Nanjing Unicorn Academy of Innovation, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Nanjing 211135, China.
² State Key Laboratory of Oncogenes and Related Genes, Center for Single-Cell Omics, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China.
³ The Center for Microbes, Development, and Health, Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China; The University of Chinese Academy of Sciences, Beijing, China.
⁴ Division of Infectious Diseases, Boston Children's Hospital/Harvard Medical School, Boston, MA, USA.
⁵ The Center for Microbes, Development, and Health, Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China.
⁶ The Center for Microbes, Development, and Health, Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Shanghai 200031, China; The Nanjing Unicorn Academy of Innovation, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Nanjing 211135, China. Electronic address: cbchen@ips.ac.cn.
⁷ State Key Laboratory of Oncogenes and Related Genes, Center for Single-Cell Omics, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China. Electronic address: liuningning@shsmu.edu.cn.

PMID: 35081357
DOI: 10.1016/j.celrep.2021.110293

Abstract

Successful host colonization by fungi in fluctuating niches requires response and adaptation to multiple environmental stresses. However, our understanding about how fungal species thrive in the gastrointestinal (GI) ecosystem by combing multifaceted nutritional stress with respect to homeostatic host-commensal interactions is still in its infancy. Here, we discover that depletion of the phosphate transceptor Pho84 across multiple fungal species encountered a substantial cost in gastrointestinal colonization. Mechanistically, Pho84 enhances the gastrointestinal commensalism via a dual-action activity, coordinating both phosphate uptake and TOR activation by induction of the transcriptional regulator Try4 and downstream commensalism-related transcription. As such, Pho84 promotes Candida albicans commensalism, but this does not translate into enhanced pathogenicity. Thus, our study uncovers a specific nutrient-dependent dual-action regulatory pathway for Pho84 on fungal commensalism.

Keywords: Candida albicans; Pho84; dual-action activity; gastrointestinal commensalism.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Caco-2 Cells
Candida albicans / metabolism*
Female
Fungal Proteins / metabolism*
Gastrointestinal Microbiome / physiology*
Humans
Mice
Mice, Inbred C57BL
Proton-Phosphate Symporters / metabolism*
Symbiosis / physiology*

Substances

Fungal Proteins
Proton-Phosphate Symporters