Functional Characterization of the Global Regulator Hfq in Aeromonas veronii Reveals an Essential Role in Pathogenesis and Secretion of Effectors

Zihui Cai; Lanjuan Guo; Juanjuan Li; Hong Li; Yanqiong Tang; Xue Chi; Zhu Liu; Xiang Ma

doi:10.1016/j.micpath.2024.107271

Functional Characterization of the Global Regulator Hfq in Aeromonas veronii Reveals an Essential Role in Pathogenesis and Secretion of Effectors

Microb Pathog. 2024 Dec 30:107271. doi: 10.1016/j.micpath.2024.107271. Online ahead of print.

Authors

Zihui Cai¹, Lanjuan Guo², Juanjuan Li³, Hong Li⁴, Yanqiong Tang⁵, Xue Chi⁶, Zhu Liu⁷, Xiang Ma⁸

Affiliations

¹ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
² Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
³ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
⁴ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
⁵ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
⁶ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].
⁷ Yunnan Provincial Key Laboratory of Animal Nutrition and Feed, Faculty of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China. Electronic address: [email protected].
⁸ Pathogenesis and Control of Pathogenic Microorganisms Research Team, School of Life and Health Sciences, Hainan Province Key Laboratory of One Health, Collaborative Innovation Center of One Health, Hainan University, Haikou, Hainan 570228, China. Electronic address: [email protected].

PMID: 39742896
DOI: 10.1016/j.micpath.2024.107271

Abstract

The RNA chaperone Hfq acts as an important virulence regulator playing a diverse role in the virulence and pathogenicity of several infectious bacteria. As a threating pathogen inducing diseases in humans, animals and aquatic organisms, Aeromonas veronii attracts attentions with respect to its elusive pathogenic mechanism and virulence factors. This study aims to elucidate the functions of hfq gene in A. veronii, and the findings reveal that it is essential for the pathogenesis of the pathogen. We demonstrated that deletion of hfq gene from A. veronii led to reduced swimming motility and diminished assemblies of surficial appendages. In addition, the capability of hfq deletion to form biofilm was 8.2-fold reduced, the adhesion to epithelial cells or ex vivo intestine was 6.0 or 1.9-fold lower, respectively, and the colonization counts in mice was attenuated about 13 fold in heart, 149 fold in liver, 81 fold in lung, and 104 fold in kidney, in relative to the wild type. Surprisingly, a higher level of secreted proteins was observed in hfq deletion and the cytotoxicity to Caco-2 cells was increased about 1.7-fold. The apparent contradiction that hfq deletion exhibits attenuated virulence characteristics but enhanced secretion and cytotoxic effects of virulent factors implies a work model showing that Hfq functions as a hub to control the energy-consuming expression of virulent factors for a balance between the virulence and fitness of the pathogen. The pleiotropic effects suggest that Hfq is a key regulator of important aspects of virulence in A. veronii and involved in the secretion of virulence factors, constituting an indispensable functional factor for the establishment of pathogenicity of A. veronii.

Keywords: Aeromonas veronii; biofilm; cell adhesion; colonization; cytotoxicity; flagella; hfq deletion; motility; pathogenesis; protein secretion; swimming; virulence.