Differential alteration in Lactiplantibacillus plantarum subsp. plantarum quorum-sensing systems and reduced Candida albicans yeast survival and virulence gene expression in dual-species interaction

Author:

Xu Zhenbo12ORCID,Li Yaqin1,Xu Aijuan3,Xue Liang145,Soteyome Thanapop6,Yuan Lei7,Ma Qin8,Seneviratne Gamini9,Hong Wei10,Mao Yuzhu11,Kjellerup Birthe V.11,Liu Junyan1213ORCID

Affiliation:

1. Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety, Engineering Research Center of Starch and Vegetable Protein Processing Ministry of Education, School of Food Science and Engineering, South China University of Technology, Guangzhou, China

2. Department of Laboratory Medicine, the Second Affiliated Hospital of Shantou University Medical College, Shantou, Guangdong, China

3. Guangzhou Hybribio Medical Laboratory, Guangzhou, China

4. Guangdong Provincial Key Laboratory of Microbial Safety and Health, State Key Laboratory of Applied Microbiology Southern China, Institute of Microbiology, Guangdong Academy of Sciences, China, Guangzhou, Guangdong

5. Key Laboratory of Agricultural Microbiomics and Precision Application, Ministry of Agriculture and Rural Affairs, Guangdong Academy of Sciences, Guangzhou, Guangdong, China

6. Home Economics Technology, Rajamangala University of Technology Phra Nakhon, Bangkok, Thailand

7. School of Food Science and Engineering, Yangzhou University, Yangzhou, Jiangsu, China

8. Key Laboratory of Functional Foods, Ministry of Agriculture, Guangdong Key Laboratory of Agricultural Products Processing, Sericultural and Agri-Food Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, China

9. National Institute of Fundamental Studies, Kandy, Sri Lanka

10. GMU-GIBH Joint School of Life Sciences, Guangzhou Medical University, Guangzhou, Guangdong, China

11. Department of Civil and Environmental Engineering, University of Maryland, College Park, Maryland, USA

12. Guangdong Provincial Key Laboratory of Lingnan Specialty Food Science and Technology, College of Light Industry and Food Science, Academy of Contemporary Agricultural Engineering Innovations, Zhongkai University of Agriculture and Engineering, Guangzhou, China

13. Key Laboratory of Green Processing and Intelligent Manufacturing of Lingnan Specialty Food, Ministry of Agriculture, Guangzhou, China

Abstract

ABSTRACT Candida albicans ( C. albicans ) and Lactiplantibacillus plantarum subsp. plantarum ( L. plantarum ) are frequently identified in various niches, but their dual-species interaction, especially with C. albicans in yeast form, remains unclear. This study aimed to investigate the dual-species interaction of L. plantarum and C. albicans , including proliferation, morphology, and transcriptomes examined by selective agar plate counting, microscopy, and polymicrobial RNA-seq, respectively. Maintaining a stable and unchanged growth rate, L. plantarum inhibited C. albicans yeast cell proliferation but not hyphal growth. Combining optical microscopy and atomic force microscopy, cell-to-cell direct contact and co-aggregation with L. plantarum cells surrounding C. albicans yeast cells were observed during dual-species interaction. Reduced C. albicans yeast cell proliferation in mixed culture was partially due to L. plantarum cell-free culture supernatant but not the acidic environment. Upon polymicrobial transcriptomics analysis, interesting changes were identified in both L. plantarum and C. albicans gene expression. First, two L. plantarum quorum-sensing systems showed contrary changes, with the activation of lamBDCA and repression of luxS . Second, the upregulation of stress response-related genes and downregulation of cell cycle, cell survival, and cell integrity-related pathways were identified in C. albicans , possibly connected to the stress posed by L. plantarum and the reduced yeast cell proliferation. Third, a large scale of pathogenesis and virulence factors were downregulated in C. albicans , indicating the potential interruption of pathogenic activities by L. plantarum . Fourth, partial metabolism and transport pathways were changed in L. plantarum and C. albicans . The information in this study might aid in understanding the behavior of L. plantarum and C. albicans in dual-species interaction. IMPORTANCE The anti- Candida albicans activity of Lactiplantibacillus plantarum has been explored in the past decades. However, the importance of C. albicans yeast form and the effect of C. albicans on L. plantarum had also been omitted. In this study, the dual-species interaction of L. plantarum and C. albicans was investigated with a focus on the transcriptomes. Cell-to-cell direct contact and co-aggregation with L. plantarum cells surrounding C. albicans yeast cells were observed. Upon polymicrobial transcriptomics analysis, interesting changes were identified, including contrary changes in two L. plantarum quorum-sensing systems and reduced cell survival-related pathways and pathogenesis determinants in C. albicans .

Funder

the Guangdong Province Key Laboratory for Green Processing of Natural Products and Product Safety

National Natural Science Foundation of China

Guangdong Major Project of Basic and Applied Basic Research

Guangdong Basic and Applied Basic Research Foundation Natural Science Foundation

Guangzhou Basic and Applied Basic Research Project

Guangdong Province Higher Education Featured Innovation Project

the Open Research Fund of State Key Laboratory of Biological Fermentation Engineering of Beer

Publisher

American Society for Microbiology

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