The role of morphological adaptability in Vibrio cholerae’s motility

ABSTRACT Vibrio cholerae, the causative agent of cholera, displays remarkable adaptability to diverse environmental conditions through morphological changes that enhance its pathogenicity and influence the global epidemiology of the disease. This study examines the motility differences between filam...

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Main Authors: Jun Xu, Keigo Abe, Toshio Kodama, Marzia Sultana, Denise Chac, Susan M. Markiewicz, Hideyuki Matsunami, Erika Kuba, Shiyu Tsunoda, Munirul Alam, Ana A. Weil, Shuichi Nakamura, Tetsu Yamashiro
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mBio
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Online Access:https://journals.asm.org/doi/10.1128/mbio.02469-24
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author Jun Xu
Keigo Abe
Toshio Kodama
Marzia Sultana
Denise Chac
Susan M. Markiewicz
Hideyuki Matsunami
Erika Kuba
Shiyu Tsunoda
Munirul Alam
Ana A. Weil
Shuichi Nakamura
Tetsu Yamashiro
author_facet Jun Xu
Keigo Abe
Toshio Kodama
Marzia Sultana
Denise Chac
Susan M. Markiewicz
Hideyuki Matsunami
Erika Kuba
Shiyu Tsunoda
Munirul Alam
Ana A. Weil
Shuichi Nakamura
Tetsu Yamashiro
author_sort Jun Xu
collection DOAJ
description ABSTRACT Vibrio cholerae, the causative agent of cholera, displays remarkable adaptability to diverse environmental conditions through morphological changes that enhance its pathogenicity and influence the global epidemiology of the disease. This study examines the motility differences between filamentous and comma-shaped forms of the V. cholerae O1 strain under various viscosity conditions. Utilizing the El Tor strain, we induced filamentous transformation and conducted a comparative analysis with the canonical comma-shaped morphology. Our methodology involved assessing motility patterns, swimming speeds, rotation rates, kinematics, and reversal frequencies using dark-field microscopy and high-speed imaging techniques. The results show that filamentous V. cholerae cells retain enhanced motility in viscous environments, indicating an evolutionary adaptation for survival in varied habitats, particularly the human gastrointestinal tract. Filamentous forms exhibited increased reversal behavior at mucin interfaces, suggesting an advantage in penetrating the mucus layer. Furthermore, the presence of filamentous cells in bile-supplemented medium underscores their relevance in natural infection scenarios.IMPORTANCEThis study highlights the enhanced motility of filamentous Vibrio cholerae in viscous environments, an adaptation that may provide a survival advantage in the human gastrointestinal tract. By demonstrating increased reversal behavior at mucin interfaces, filamentous V. cholerae cells exhibit a superior ability to penetrate the mucus layer, which is crucial for effective colonization and infection. Filamentous cells in bile-supplemented media further underscores their potential role in disease pathogenesis. These findings offer critical insights into the morphological flexibility of V. cholerae and its potential implications for infection dynamics, paving the way for more effective strategies in managing and preventing cholera outbreaks.
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spelling doaj-art-b14cfb8b8ddb4670a084445602892a9c2025-01-08T14:00:38ZengAmerican Society for MicrobiologymBio2150-75112025-01-0116110.1128/mbio.02469-24The role of morphological adaptability in Vibrio cholerae’s motilityJun Xu0Keigo Abe1Toshio Kodama2Marzia Sultana3Denise Chac4Susan M. Markiewicz5Hideyuki Matsunami6Erika Kuba7Shiyu Tsunoda8Munirul Alam9Ana A. Weil10Shuichi Nakamura11Tetsu Yamashiro12Department of Bacteriology, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, JapanDepartment of Applied Physics, Graduate School of Engineering, Tohoku University, Sendai, Miyagi, JapanDepartment of Bacteriology, Institute of Tropical Medicine, Nagasaki University, Nagasaki, JapanInfectious Diseases Division, International Center for Diarrheal Disease Research, Bangladesh, Bangladesh, DhakaDepartment of Medicine, University of Washington, Seattle, Washington, USADepartment of Medicine, University of Washington, Seattle, Washington, USAMolecular Cryo-Electron Microscopy Unit, Okinawa Institute of Science and Technology, Okinawa, JapanDepartment of Bacteriology, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, JapanDepartment of Bacteriology, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, JapanInfectious Diseases Division, International Center for Diarrheal Disease Research, Bangladesh, Bangladesh, DhakaDepartment of Medicine, University of Washington, Seattle, Washington, USADepartment of Applied Physics, Graduate School of Engineering, Tohoku University, Sendai, Miyagi, JapanDepartment of Bacteriology, Graduate School of Medicine, University of the Ryukyus, Nishihara, Okinawa, JapanABSTRACT Vibrio cholerae, the causative agent of cholera, displays remarkable adaptability to diverse environmental conditions through morphological changes that enhance its pathogenicity and influence the global epidemiology of the disease. This study examines the motility differences between filamentous and comma-shaped forms of the V. cholerae O1 strain under various viscosity conditions. Utilizing the El Tor strain, we induced filamentous transformation and conducted a comparative analysis with the canonical comma-shaped morphology. Our methodology involved assessing motility patterns, swimming speeds, rotation rates, kinematics, and reversal frequencies using dark-field microscopy and high-speed imaging techniques. The results show that filamentous V. cholerae cells retain enhanced motility in viscous environments, indicating an evolutionary adaptation for survival in varied habitats, particularly the human gastrointestinal tract. Filamentous forms exhibited increased reversal behavior at mucin interfaces, suggesting an advantage in penetrating the mucus layer. Furthermore, the presence of filamentous cells in bile-supplemented medium underscores their relevance in natural infection scenarios.IMPORTANCEThis study highlights the enhanced motility of filamentous Vibrio cholerae in viscous environments, an adaptation that may provide a survival advantage in the human gastrointestinal tract. By demonstrating increased reversal behavior at mucin interfaces, filamentous V. cholerae cells exhibit a superior ability to penetrate the mucus layer, which is crucial for effective colonization and infection. Filamentous cells in bile-supplemented media further underscores their potential role in disease pathogenesis. These findings offer critical insights into the morphological flexibility of V. cholerae and its potential implications for infection dynamics, paving the way for more effective strategies in managing and preventing cholera outbreaks.https://journals.asm.org/doi/10.1128/mbio.02469-24Vibrio choleraebacterial filamentationbacterial motilitymucus penetration
spellingShingle Jun Xu
Keigo Abe
Toshio Kodama
Marzia Sultana
Denise Chac
Susan M. Markiewicz
Hideyuki Matsunami
Erika Kuba
Shiyu Tsunoda
Munirul Alam
Ana A. Weil
Shuichi Nakamura
Tetsu Yamashiro
The role of morphological adaptability in Vibrio cholerae’s motility
mBio
Vibrio cholerae
bacterial filamentation
bacterial motility
mucus penetration
title The role of morphological adaptability in Vibrio cholerae’s motility
title_full The role of morphological adaptability in Vibrio cholerae’s motility
title_fullStr The role of morphological adaptability in Vibrio cholerae’s motility
title_full_unstemmed The role of morphological adaptability in Vibrio cholerae’s motility
title_short The role of morphological adaptability in Vibrio cholerae’s motility
title_sort role of morphological adaptability in vibrio cholerae s motility
topic Vibrio cholerae
bacterial filamentation
bacterial motility
mucus penetration
url https://journals.asm.org/doi/10.1128/mbio.02469-24
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