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Transitioning to confined spaces impacts bacterial swimming and escape response

View ORCID ProfileJonathan B. Lynch, Nicholas James, Margaret McFall-Ngai, Edward G. Ruby, View ORCID ProfileSangwoo Shin, View ORCID ProfileDaisuke Takagi
doi: https://doi.org/10.1101/2021.09.15.460467
Jonathan B. Lynch
1Pacific Biosciences Research Center, University of Hawai‘i at Mānoa, Honolulu, HI, USA
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  • For correspondence: jblynch@g.ucla.edu
Nicholas James
2Department of Cell and Molecular Biology, University of Hawai‘i at Mānoa, Honolulu, HI, USA
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Margaret McFall-Ngai
1Pacific Biosciences Research Center, University of Hawai‘i at Mānoa, Honolulu, HI, USA
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Edward G. Ruby
1Pacific Biosciences Research Center, University of Hawai‘i at Mānoa, Honolulu, HI, USA
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Sangwoo Shin
3Department of Mechanical Engineering, University of Hawai‘i at Mānoa, Honolulu, HI, USA
4Department of Mechanical and Aerospace Engineering, University at Buffalo, Buffalo, NY, USA
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Daisuke Takagi
1Pacific Biosciences Research Center, University of Hawai‘i at Mānoa, Honolulu, HI, USA
3Department of Mechanical Engineering, University of Hawai‘i at Mānoa, Honolulu, HI, USA
5Department of Mathematics, University of Hawai‘i-Mānoa, Honolulu, HI, USA
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Abstract

Symbiotic bacteria often navigate complex environments before colonizing privileged sites in their host organism. Chemical gradients are known to facilitate directional taxis of these bacteria, guiding them towards their eventual destination. However, less is known about the role of physical features in shaping the path the bacteria take and defining how they traverse a given space. The flagellated marine bacterium Vibrio fischeri,which forms a binary symbiosis with the Hawaiian bobtail squid, Euprymna scolopes, must navigate tight physical confinement, squeezing through a bottleneck constricting to ~2 μm in width on the way to its eventual home. Using microfluidic in vitro experiments, we discovered that V. fischeri cells alter their behavior upon entry into confined space, straightening their swimming paths and promoting escape from confinement. Using a computational model, we attributed this escape response to two factors: reduced directional fluctuation and a refractory period between reversals. Additional experiments in asymmetric capillary tubes confirmed that V. fischeri quickly escape from tapered ends, even when drawn into the ends by chemoattraction. This avoidance was apparent down to a limit of confinement approaching the diameter of the cell itself, resulting in a balance between chemoattraction and evasion of physical confinement. Our findings demonstrate that non-trivial distributions of swimming bacteria can emerge from simple physical gradients in the level of confinement. Tight spaces may serve as an additional, crucial cue for bacteria while they navigate complex environments to enter specific habitats.

Significance Statement Symbiotic bacteria that navigate to and through specific host tissues often face tight physical confinement. This work reveals that confinement-associated changes in swimming can dramatically alter taxis, shaping bacterial localization in conjuncture with other motility-directing cues. This work helps explain how bacteria can avoid getting stuck in confined areas while transiting to privileged spaces, adding confinement as an environmental cue that symbiotic bacteria use to shape their motility behavior.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Added supplementary text file and additional reference in introduction

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 21, 2021.
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Transitioning to confined spaces impacts bacterial swimming and escape response
Jonathan B. Lynch, Nicholas James, Margaret McFall-Ngai, Edward G. Ruby, Sangwoo Shin, Daisuke Takagi
bioRxiv 2021.09.15.460467; doi: https://doi.org/10.1101/2021.09.15.460467
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Transitioning to confined spaces impacts bacterial swimming and escape response
Jonathan B. Lynch, Nicholas James, Margaret McFall-Ngai, Edward G. Ruby, Sangwoo Shin, Daisuke Takagi
bioRxiv 2021.09.15.460467; doi: https://doi.org/10.1101/2021.09.15.460467

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