Mechanical shear controls bacterial penetration in mucus

Figueroa-Morales, Nuris; Dominguez-Rubio, Leonardo; Ott, Troy L.; Aranson, Igor S.

doi:10.1038/s41598-019-46085-z

Cited by 41 publications

(47 citation statements)

References 58 publications

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“…It is also believed that the helical cell shape of both H. pylori and Campylobacter jejuni , which colonizes the thick mucus layer of the cecum, facilitates mucus penetration by allowing the body to push against the mucin matrix like a corkscrew ( 34 , 35 ). Recent work demonstrated that the peritrichous rod-shaped bacteria Escherichia coli and Bacillus subtilis can penetrate cervical mucus by taking advantage of water channels created by shear forces during secretion ( 36 ). The behavior of V. cholerae in mucus has not been described.…”

Section: Introductionmentioning

confidence: 99%

Alkaline pH Increases Swimming Speed and Facilitates Mucus Penetration for Vibrio cholerae

et al. 2021

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Intestinal mucus is the first line of defense against intestinal pathogens. It acts as a physical barrier between epithelial tissues and the lumen that enteropathogens must overcome to establish a successful infection. We investigated the motile behavior of two V. cholerae strains (El Tor C6706 and Classical O395) in mucus using single cell tracking in unprocessed porcine intestinal mucus. We determined that V. cholerae is able to penetrate mucus using flagellar motility and that alkaline pH increases swimming speed, and consequently, improves mucus penetration. Microrheological measurements indicate that changes in pH between 6 and 8 (the physiological range for the human small intestine) had little effect on the viscoelastic properties of mucus. Finally, we determined that acidic pH promotes surface attachment by activating the mannose-sensitive haemagglutinin (MshA) pilus in V. cholerae El Tor C6706 without a measurable change in the total cellular concentration of the secondary messenger cyclic dimeric guanosine monophosphate (c-di-GMP). Overall, our results support that pH is an important factor affecting the motile behavior of V. cholerae and its ability to penetrate mucus. Therefore, changes in pH along the human small intestine may play a role in determining the preferred site for V. cholerae during infection. IMPORTANCE The diarrheal disease cholera is still a burden for populations in developing countries with poor sanitation. To develop effective vaccines and prevention strategies against Vibrio cholerae, we must understand the initial steps of infection leading to the colonization of the small intestine. To infect the host and deliver the cholera toxin, V. cholerae has to penetrate the mucus layer protecting the intestinal tissues. However, the interaction of V. cholerae with intestinal mucus has not been extensively investigated. In this report, we demonstrated using single cell tracking that V. cholerae is able to penetrate intestinal mucus using flagellar motility. In addition, we observed that alkaline pH improves the ability of V. cholerae to penetrate mucus. This finding has important implications for understanding the dynamics of infection because pH varies significantly along the small intestine, between individuals, and between species. Blocking mucus penetration by interfering with flagellar motility in V. cholerae, reinforcing the mucosa, controlling intestinal pH, or manipulating the intestinal microbiome, will offer new strategies to fight cholera.

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Section: Introductionmentioning

confidence: 99%

Alkaline pH Increases Swimming Speed and Facilitates Mucus Penetration for Vibrio cholerae

et al. 2021

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“…Furthermore, many biological fluids, such as mucus, DNA solutions, or suspensions of long viruses exhibit a certain degree of liquid crystallinity [12][13][14][15][16] . Liquid crystallinity and mechanical shear also can control bacteria penetration in mucus 17 . Besides the theoretical importance, studies of bacteria motility in complex fluids provide clues in the propagation of bacteria-born diseases and colonization of tissues by pathogens.…”

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confidence: 99%

Surface anchoring controls orientation of a microswimmer in nematic liquid crystal

et al. 2020

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Microscopic swimmers, both living and synthetic, often dwell in anisotropic viscoelastic environments. The most representative realization of such an environment is water-soluble liquid crystals. Here, we study how the local orientation order of liquid crystal affects the motion of a prototypical elliptical microswimmer. In the framework of well-validated Beris-Edwards model, we show that the microswimmer’s shape and its surface anchoring strength affect the swimming direction and can lead to reorientation transition. Furthermore, there exists a critical surface anchoring strength for non-spherical bacteria-like microswimmers, such that swimming occurs perpendicular in a sub-critical case and parallel in super-critical case. Finally, we demonstrate that for large propulsion speeds active microswimmers generate topological defects in the bulk of the liquid crystal. We show that the location of these defects elucidates how a microswimmer chooses its swimming direction. Our results can guide experimental works on control of bacteria transport in complex anisotropic environments.

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“…Bacterial penetration into meat and leafy vegetables with sessile drops were mathematically modeled previously (22)(23)(24). Bacterial migration in colon mucus and to the epithelial layer was investigated (25). The effect of chemotaxis on host infection and pathogenicity was also reviewed (26).…”

Section: Literature About Mathematical Modeling and Experimental Studies Of Bacterial Penetration In The Gastrointestinal Tractmentioning

confidence: 99%

Migration of aerobic bacteria from the duodenum to the pancreas with tumors: a mechanistic understanding

Shirai

Ito

Tsukada

2021

Preprint

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More aerobic bacteria are found in the pancreas with tumors than in the healthy pancreas. We provide a mechanistic understanding of the migration of intestinal bacteria from the duodenum to the pancreas with tumors. Mathematical models of migration of aerobic bacteria from the duodenum to the pancreas with tumors in the hepatopancreatic duct were developed. In addition, the behaviors of GFP E. coli under a pH gradient in a microfluidic device were analyzed. Moreover, upstream migrations of Pseudomonas fluorescens against flow were measured in a polydimethylsiloxane (PDMS) T-shaped cylinder mimicking a pancreatic duct. The simulated bacterial concentration of the pancreas with tumors was higher than that of the healthy pancreas and agreed reasonably well with the literature. Migration of aerobic bacteria in the hepatopancreatic duct is counteracted by bile and pancreatic juice flow but facilitated greatly by bacterial pH taxis from lower pH in duodenum fluid toward slightly alkaline pH in pancreatic juice, favorable for them. Migration of bacteria to the pancreas with tumors is made easier by solid tumors on the pancreatic duct, which compresses the pancreatic duct and thus reduces the fluid flow rate. On the other hand, GFP E. coli migrated under the pH gradient in a microfluidic device from acidic areas toward neutral or slightly alkaline pH, validating pH taxis. Furthermore, Pseudomonas fluorescens migrated upstream from hydrochloride solution but not from bicarbonate solution against bicarbonate flow at >20 µm/s, with an advancing velocity of approximately 60 µm/s, validating the models (244 words).

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Mechanical shear controls bacterial penetration in mucus

Cited by 41 publications

References 58 publications

Alkaline pH Increases Swimming Speed and Facilitates Mucus Penetration for Vibrio cholerae

Alkaline pH Increases Swimming Speed and Facilitates Mucus Penetration for Vibrio cholerae

Surface anchoring controls orientation of a microswimmer in nematic liquid crystal

Migration of aerobic bacteria from the duodenum to the pancreas with tumors: a mechanistic understanding

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