Class A Penicillin-Binding Protein C Is Responsible for Stress Response by Regulation of Peptidoglycan Assembly in Clavibacter michiganensis

Xing Chen; Yao Li; Kaihong Bai; Meng Gu; Xiaoli Xu; Na Jiang; Yu Chen; Jianqiang Li; Laixin Luo

doi:10.1128/spectrum.01816-22

Microbiology Spectrum (Oct 2022)

Class A Penicillin-Binding Protein C Is Responsible for Stress Response by Regulation of Peptidoglycan Assembly in Clavibacter michiganensis

Xing Chen,
Yao Li,
Kaihong Bai,
Meng Gu,
Xiaoli Xu,
Na Jiang,
Yu Chen,
Jianqiang Li,
Laixin Luo

Affiliations

Xing Chen: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Yao Li: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Kaihong Bai: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Meng Gu: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Xiaoli Xu: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Na Jiang: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Yu Chen: Key Laboratory of Integrated Crop Pest Management of Anhui Province, Key Laboratory of Biology and Sustainable Management of Plant Diseases and Pests of Anhui Higher Education Institutes, School of Plant Protection, Anhui Agricultural University, Hefei, People’s Republic of China
Jianqiang Li: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China
Laixin Luo: Department of Plant Pathology and MOA Key Laboratory of Pest Monitoring and Green Management, College of Plant Protection, Beijing Key Laboratory of Seed Disease Testing and Control, China Agricultural University, Beijing, People’s Republic of China

DOI: https://doi.org/10.1128/spectrum.01816-22
Journal volume & issue: Vol. 10, no. 5

Abstract

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ABSTRACT The cell wall peptidoglycan of bacteria is essential for their survival and shape development. The penicillin-binding proteins (PBPs) are responsible for the terminal stage of peptidoglycan assembly. It has been shown that PBPC, a member of class A high-molecular-weight PBP, played an important role in morphology maintenance and stress response in Clavibacter michiganensis. Here, we reported the stress response strategies under viable but nonculturable (VBNC) state and revealed the regulation of peptidoglycan assembly by PBPC in C. michiganensis cells. Using atomic force microscopy imaging, we found that peptidoglycan of C. michiganensis cells displayed a relatively smooth and dense surface, whereas ΔpbpC was characterized by a “ridge-and-groove” surface, which was more distinctive after Cu2+ treatment. The peptidoglycan layer of wild type cells exhibited a significant increase in thickness and slight increase in cross-linkage following Cu2+ treatment. Compared with wild type, the thickness and cross-linkage of peptidoglycan decreased during log phase in ΔpbpC cells, but the peptidoglycan cross-linkage increased significantly under Cu2+ stress, while the thickness did not change. It is noteworthy that the above changes in the peptidoglycan layer resulted in a significant increase in the accumulation of amylase and exopolysaccharide in ΔpbpC. This study elucidates the role of PBPC in Gram-positive rod-shaped plant pathogenic bacterium in response to environmental stimuli by regulating the assembling of cell wall peptidoglycan, which is significant in understanding the survival of C. michiganensis under stress and the field epidemiology of tomato bacterial canker disease. IMPORTANCE Peptidoglycan of cell walls in bacteria is a cross-linked and meshlike scaffold that provides strength to withstand the external pressure. The increased cross-linkage in peptidoglycan and altered structure in VBNC cells endowed the cell wall more resistant to adversities. Here we systematically evaluated the stress response strategies in Gram-positive rod-shaped bacterium C. michiganensis log phase cells and revealed a significant increase of peptidoglycan thickness and slight increase of cross-linkage after Cu2+ treatment. Most strikingly, knocking-out of PBPC leads to a significant increase in cross-linking of peptidoglycan in response to Cu2+ treatment. Understanding the stress resistance mechanism and survival strategy of phytopathogenic bacteria is the basis of exploring bacterial physiology and disease epidemiology.

Published in Microbiology Spectrum

ISSN: 2165-0497 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/spectrum

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