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Insertion of a Divergent GAF-like Domain Defines a Novel Family of YcgR Homologues That Bind c-di-GMP in Leptospirales

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Visnardi, Aline Biazola ; Ribeiro, Rodolfo Alvarenga ; de Souza, Anacleto Silva ; Vinces, Tania Geraldine Churasacari ; Llontop, Edgar E. ; Ferrari, Anielle Salviano de Almeida ; Henrique, Pedro Antonio Franca ; Valdivieso, Daniela ; Sanchez-Limache, Daniel Enrique ; Silva, Gabriela Roberto ; Soares, Eduardo Pereira ; Santos, Thomas Wittmann Cezar ; Farah, Chuck Shaker ; Sassonia, Rogerio Corte ; Salinas, Roberto K. ; Guzzo, Cristiane Rodrigues ; de Souza, Robson Francisco
Total Authors: 17
Document type: Journal article
Source: ACS OMEGA; v. 10, n. 4, p. 19-pg., 2025-01-21.
Abstract

The Leptospiraceae family, which includes the genera Leptospira, Leptonema, and Turneriella, is an ecologically diverse group that includes saprophytic strains from soil and water as well as important pathogenic strains. Adaptation to these multiple environments relies strongly on signal transduction to adjust their morphology, motility, and metabolism to the changing environmental conditions. Members of the genus Leptospira distinguish themselves among spirochetes for having an elevated number of signal transduction genes. In this study, we describe a novel signal transduction protein that has gained multiple paralogues in the Leptospiraceae. These proteins are members of the YcgR/DgrA/MotI family, whose orthologs in several bacterial lineages have been shown to regulate the flagellar motor upon binding to c-di-GMP through their N-terminal PilZ domain. Unlike previously described versions of YcgR, the spirochetal proteins are characterized by the insertion of a divergent GAF domain within their N-terminal PilZ domain. We show that one member of this protein family from Leptospira interrogans is still a monomeric c-di-GMP binding protein and that these novel YcgR-like proteins have mostly replaced other members of the YcgR family in Leptospiraceae. Marked divergence among the paralogs suggests this family's expansion was accompanied by neofunctionalization, with the likely emergence of novel interactions in the signal transduction network controlling the flagellum rotor and other processes affected by changes in levels of c-di-GMP. (AU)

FAPESP's process: 20/04680-0 - Design of different fragments of SARS-CoV-2 surface protein spike for the development of fast diagnostic test and vaccine
Grantee:Cristiane Rodrigues Guzzo Carvalho
Support Opportunities: Regular Research Grants
FAPESP's process: 19/00195-2 - Understanding the c-di-GMP signaling networks and the Type II secretion system present into the human pathogen Leptospira interrogans Copenhageni
Grantee:Cristiane Rodrigues Guzzo Carvalho
Support Opportunities: Regular Research Grants
FAPESP's process: 21/05262-0 - Study of c-di-GMP signaling involving LIC_11920 in Leptospira interrogans
Grantee:Aline Biazola Visnardi
Support Opportunities: Scholarships in Brazil - Doctorate (Direct)
FAPESP's process: 21/00070-5 - Annual resource application plan for supporting institutional research infrastructure (ICB-USP 2018-2019)
Grantee:Carlos Pelleschi Taborda
Support Opportunities: Research Grants - Technical Reserve for Institutional Research Infrastructure
FAPESP's process: 21/10577-0 - Biology of Bacteria and Bacteriophages Research Center
Grantee:Shaker Chuck Farah
Support Opportunities: Research Grants - Research, Innovation and Dissemination Centers - RIDC
FAPESP's process: 17/17303-7 - Structure and function of bacterial secretion systems
Grantee:Shaker Chuck Farah
Support Opportunities: Research Projects - Thematic Grants
FAPESP's process: 23/10432-7 - Functional studies of VirB2 homology from Staphylococcus aureus
Grantee:Pedro Antônio França Henrique
Support Opportunities: Scholarships in Brazil - Scientific Initiation
FAPESP's process: 17/06394-1 - Muti-user equipment approved in grant 2014/22136-4: isothermal titration calorimeter (ITC) for the determination of thermodynamic parameters of molecular interactions
Grantee:Omar Abou El Seoud
Support Opportunities: Multi-user Equipment Program
FAPESP's process: 16/09047-8 - Comparative genomics of bacterial toxins associated with type IV secretion systems
Grantee:Robson Francisco de Souza
Support Opportunities: Regular Research Grants
FAPESP's process: 23/18211-0 - High-throughput virtual screening in the design of main protease inhibitors of the novel coronavirus
Grantee:Anacleto Silva de Souza
Support Opportunities: Scholarships in Brazil - Post-Doctoral
FAPESP's process: 22/08730-7 - Protein structural biology applied in the study of c-di-GMP signaling and bacterial secretion systems
Grantee:Cristiane Rodrigues Guzzo Carvalho
Support Opportunities: Regular Research Grants