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Article

Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae. 1. Internal Structure of the Biofilm

by
Keiko Sato
1,*,
Masami Naya
2,
Yuri Hatano
2,
Yoshio Kondo
3,
Mari Sato
2,
Keiji Nagano
4,
Shicheng Chen
5,
Mariko Naito
1 and
Chikara Sato
2,*
1
Department of Microbiology and Oral Infection, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki 852-8588, Japan
2
Health and Medical Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan
3
Department of Pediatric Dentistry, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki 852-8588, Japan
4
Department of Microbiology, Health Sciences University of Hokkaido, 1757 Kanazawa, Tobetsu-cho, Ishikari-gun, Hokkaido 061-0293, Japan
5
Department of Clinical and Diagnostic Sciences, School of Health Sciences, Oakland University, 433 Meadow Brook Road, Rochester, MI 48309, USA
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(4), 1894; https://doi.org/10.3390/ijms22041894
Submission received: 15 December 2020 / Revised: 3 February 2021 / Accepted: 3 February 2021 / Published: 14 February 2021
(This article belongs to the Special Issue Liquid-Phase Electron Microscopy in Biological Applications and Material Sciences)
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Abstract

The Gram-negative bacterium Flavobacterium johnsoniae employs gliding motility to move rapidly over solid surfaces. Gliding involves the movement of the adhesin SprB along the cell surface. F. johnsoniae spreads on nutrient-poor 1% agar-PY2, forming a thin film-like colony. We used electron microscopy and time-lapse fluorescence microscopy to investigate the structure of colonies formed by wild-type (WT) F. johnsoniae and by the sprB mutant (ΔsprB). In both cases, the bacteria were buried in the extracellular polymeric matrix (EPM) covering the top of the colony. In the spreading WT colonies, the EPM included a thick fiber framework and vesicles, revealing the formation of a biofilm, which is probably required for the spreading movement. Specific paths that were followed by bacterial clusters were observed at the leading edge of colonies, and abundant vesicle secretion and subsequent matrix formation were suggested. EPM-free channels were formed in upward biofilm protrusions, probably for cell migration. In the nonspreading ΔsprB colonies, cells were tightly packed in layers and the intercellular space was occupied by less matrix, indicating immature biofilm. This result suggests that SprB is not necessary for biofilm formation. We conclude that F. johnsoniae cells use gliding motility to spread and maturate biofilms.
Keywords: extracellular polymeric matrix; extracellular fibers; vesicle; bacterial clusters; cell-to-cell connections; transmission electron microscopy extracellular polymeric matrix; extracellular fibers; vesicle; bacterial clusters; cell-to-cell connections; transmission electron microscopy
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MDPI and ACS Style

Sato, K.; Naya, M.; Hatano, Y.; Kondo, Y.; Sato, M.; Nagano, K.; Chen, S.; Naito, M.; Sato, C. Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae. 1. Internal Structure of the Biofilm. Int. J. Mol. Sci. 2021, 22, 1894. https://doi.org/10.3390/ijms22041894

AMA Style

Sato K, Naya M, Hatano Y, Kondo Y, Sato M, Nagano K, Chen S, Naito M, Sato C. Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae. 1. Internal Structure of the Biofilm. International Journal of Molecular Sciences. 2021; 22(4):1894. https://doi.org/10.3390/ijms22041894

Chicago/Turabian Style

Sato, Keiko, Masami Naya, Yuri Hatano, Yoshio Kondo, Mari Sato, Keiji Nagano, Shicheng Chen, Mariko Naito, and Chikara Sato. 2021. "Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae. 1. Internal Structure of the Biofilm" International Journal of Molecular Sciences 22, no. 4: 1894. https://doi.org/10.3390/ijms22041894

APA Style

Sato, K., Naya, M., Hatano, Y., Kondo, Y., Sato, M., Nagano, K., Chen, S., Naito, M., & Sato, C. (2021). Biofilm Spreading by the Adhesin-Dependent Gliding Motility of Flavobacterium johnsoniae. 1. Internal Structure of the Biofilm. International Journal of Molecular Sciences, 22(4), 1894. https://doi.org/10.3390/ijms22041894

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