Lemon exosome-like nanoparticles enhance stress survival of gut bacteria by RNase P-mediated specific tRNA decay

Chao Lei; Yun Teng; Liqing He; Mohammed Sayed; Jingyao Mu; Fangyi Xu; Xiangcheng Zhang; Anil Kumar; Kumaran Sundaram; Mukesh K Sriwastva; Lifeng Zhang; Shao-Yu Chen; Wenke Feng; Shuangqin Zhang; Jun Yan; Juw Won Park; Michael L Merchant; Xiang Zhang; Huang-Ge Zhang

doi:10.1016/j.isci.2021.102511

Lemon exosome-like nanoparticles enhance stress survival of gut bacteria by RNase P-mediated specific tRNA decay

iScience. 2021 May 5;24(6):102511. doi: 10.1016/j.isci.2021.102511. eCollection 2021 Jun 25.

Authors

Chao Lei^{1

2}, Yun Teng¹, Liqing He³, Mohammed Sayed⁴, Jingyao Mu¹, Fangyi Xu¹, Xiangcheng Zhang⁵, Anil Kumar¹, Kumaran Sundaram¹, Mukesh K Sriwastva¹, Lifeng Zhang¹, Shao-Yu Chen⁶, Wenke Feng², Shuangqin Zhang⁷, Jun Yan¹, Juw Won Park^{4

8}, Michael L Merchant³, Xiang Zhang³, Huang-Ge Zhang^{9

1}

Affiliations

¹ James Graham Brown Cancer Center, Department of Microbiology & Immunology, University of Louisville, CTRB 309 505 Hancock Street, Louisville, KY 40202, USA.
² Department of Medicine, University of Louisville, Louisville, KY 40202, USA.
³ Kidney Disease Program and Clinical Proteomics Center, University of Louisville, Louisville, KY, USA.
⁴ Department of Computer Engineering and Computer Science, University of Louisville, Louisville, KY 40202, USA.
⁵ Department of ICU, the Affiliated Huaian NO.1 People's Hospital of Nanjing Medical University, Huaian, Jiangsu 223300, China.
⁶ Department of Pharmacology and Toxicology, University of Louisville, Louisville, KY 40202, USA.
⁷ Peeples Cancer Institute, 215 Memorial Drive, Dalton, GA 30720, USA.
⁸ KBRIN Bioinformatics Core, University of Louisville, Louisville, KY 40202, USA.
⁹ Robley Rex Veterans Affairs Medical Center, Louisville, KY 40206, USA.

Abstract

Diet and bile play critical roles in shaping gut microbiota, but the molecular mechanism underlying interplay with intestinal microbiota is unclear. Here, we showed that lemon-derived exosome-like nanoparticles (LELNs) enhance lactobacilli toleration to bile. To decipher the mechanism, we used Lactobacillus rhamnosus GG (LGG) as proof of concept to show that LELNs enhance LGG bile resistance via limiting production of Msp1 and Msp3, resulting in decrease of bile accessibility to cell membrane. Furthermore, we found that decline of Msps protein levels was regulated through specific tRNA_ser ^UCC and tRNA_ser ^UCG decay. We identified RNase P, an essential housekeeping endonuclease, being responsible for LELNs-induced tRNA_ser ^UCC and tRNA_ser ^UCG decay. We further identified galacturonic acid-enriched pectin-type polysaccharide as the active factor in LELNs to increase bile resistance and downregulate tRNA_ser ^UCC and tRNA_ser ^UCG level in the LGG. Our study demonstrates a tRNA-based gene expression regulation mechanism among lactobacilli to increase bile resistance.

Keywords: Microbiology; Molecular biology; Nanoparticles.

Abstract

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