CsgI (YccT) Is a Novel Inhibitor of Curli Fimbriae Formation in Escherichia coli Preventing CsgA Polymerization and Curli Gene Expression

Author:

Sano Kotaro12ORCID,Kobayashi Hiroaki12ORCID,Chuta Hirotaka12,Matsuyoshi Nozomi12,Kato Yuki12,Ogasawara Hiroshi1345ORCID

Affiliation:

1. Research Center for Advanced Science and Technology, Division of Gene Research, Shinshu University, 3-15-1 Ueda, Nagano 386-8567, Japan

2. Department of Applied Biology, Graduated School of Science and Technology, Shinshu University, 3-15-1 Ueda, Nagano 386-8567, Japan

3. Academic Assembly School of Humanities and Social Sciences Institute of Humanities, Shinshu University, Matsumoto 390-8621, Japan

4. Institute for Fiber Engineering (IFES), Interdisciplinary Cluster for Cutting Edge Research (ICCER), Shinshu University, Tokida 3-15-1, Ueda, Nagano 386-8567, Japan

5. Renaissance Center for Applied Microbiology, Shinshu University, Nagano-shi, Nagano 380-8553, Japan

Abstract

Curli fimbriae are amyloids—found in bacteria (Escherichia coli)—that are involved in solid-surface adhesion and bacterial aggregation during biofilm formation. The curli protein CsgA is coded by a csgBAC operon gene, and the transcription factor CsgD is essential to induce its curli protein expression. However, the complete mechanism underlying curli fimbriae formation requires elucidation. Herein, we noted that curli fimbriae formation was inhibited by yccT—i.e., a gene that encodes a periplasmic protein of unknown function regulated by CsgD. Furthermore, curli fimbriae formation was strongly repressed by CsgD overexpression caused by a multicopy plasmid in BW25113—the non-cellulose-producing strain. YccT deficiency prevented these CsgD effects. YccT overexpression led to intracellular YccT accumulation and reduced CsgA expression. These effects were addressed by deleting the N-terminal signal peptide of YccT. Localization, gene expression, and phenotypic analyses revealed that YccT-dependent inhibition of curli fimbriae formation and curli protein expression was mediated by the two-component regulatory system EnvZ/OmpR. Purified YccT inhibited CsgA polymerization; however, no intracytoplasmic interaction between YccT and CsgA was detected. Thus, YccT—renamed CsgI (curli synthesis inhibitor)—is a novel inhibitor of curli fimbriae formation and has a dual role as an OmpR phosphorylation modulator and CsgA polymerization inhibitor.

Funder

Research Funds from Shinshu University

MEXT (Ministry of Education, Culture, Sports, Science and Technology of Japan) Grants-in-Aid for Young Scientists

MEXT Grants-in-Aid for Scientific Research

Publisher

MDPI AG

Subject

Inorganic Chemistry,Organic Chemistry,Physical and Theoretical Chemistry,Computer Science Applications,Spectroscopy,Molecular Biology,General Medicine,Catalysis

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