Motility of Different Gastric Helicobacter spp

Abstract

Helicobacter spp., including the well-known human gastric pathogen H. pylori, can cause gastric diseases in humans and other mammals. They are Gram-negative bacteria that colonize the gastric epithelium and use their multiple flagella to move across the protective gastric mucus layer. The flagella of different Helicobacter spp. vary in their location and number. This review focuses on the swimming characteristics of different species with different flagellar architectures and cell shapes. All Helicobacter spp. use a run-reverse-reorient mechanism to swim in aqueous solutions, as well as in gastric mucin. Comparisons of different strains and mutants of H. pylori varying in cell shape and the number of flagella show that their swimming speed increases with an increasing number of flagella and is somewhat enhanced with a helical cell body shape. The swimming mechanism of H. suis, which has bipolar flagella, is more complex than that of unipolar H. pylori. H. suis exhibits multiple modes of flagellar orientation while swimming. The pH-dependent viscosity and gelation of gastric mucin significantly impact the motility of Helicobacter spp. In the absence of urea, these bacteria do not swim in mucin gel at pH < 4, even though their flagellar bundle rotates.

Keywords: H. cetorum; H. pylori; H. suis; Helicobacter; bipolar bacteria; flagella; gastric mucin; motility; unipolar bacteria.

Figure 1

TEM images of different Helicobacter spp. showing flagella at different locations on the cell body. (A) H. pylori, scale bar 1 μm [4]. (B) H. suis, scale bar 2 μm. The flagella at the lower end are not fully visible in the image [5]. (C) H. cetorum, scale bar 0.5 μm [6]. (D) H. mustalae, scale bar 0.5 μm [7]. The images are reproduced from references [4,5,6,7] under Creative Commons Attribution 4.0 International Licenses.

Figure 2

Imaging the detailed motion of a single H. pylori bacterium. (A). The rotation of the cell body of H. pylori is shown by the change in the orientation of successive images of a swimming bacterium. For visual clarity, only the contours are outlined. The inset shows a single bacterium with its contour (blue), central axis (red), and flagellar junction J, outlined using image-analysis tools. (B). Consecutive frames of images recorded at 200 fps showing the rotation of the flagellar bundle with a rotation rate of ~66 Hz. The scale bar on both the inset to A and the 4th frame of B is 1 μm. Figure adapted from [49] © The Authors, some rights reserved; exclusive licensee AAAS. Distributed under a Creative Commons Attribution Non Commercial License 4.0 (CC BY-NC).

Figure 3

H. suis bacterium corresponding to either an extended (E) or a wrapped (W) configuration of the flagellar bundle. The EE mode corresponds to both bundles extended, EW to one extended and the other wrapped, and WW to both wrapped. Adapted from Constantino [57] under a Creative Commons Attribution 4.0 International License.

Figure 4

Swimming of H. cetorum in culture broth BB10. (A) A single frame from the movie shows several bacteria and the contour outlining one of them. (B) Trajectories of individual runs. The trajectories were randomly distributed over the figure for better visualization and do not depict the real position in the movie. (C) Time-dependent variation of the alignment angle of the center axis of the body relative to the x-axis (arbitrarily defined in the movie). The alignment angle values were shifted along the y-axis for better visualization. Adapted from Constantino [59].

Figure 5

Dot plots of the measured motility and shape parameters for H. pylori in blue (HP), H. suis in green (HS), and H. cetorum in orange (HC) swimming in BB10 broth. The horizontal lines indicate the mean and the vertical lines indicate the standard deviation. (A) Average speed, V for each run. (B) Body rotation rate, Ω for each run. (C) Distance traveled per revolution, V/Ω, for each run. (D) Body length, L of each bacterium. (E) Body diameter, d of each bacterium. (F) Body pitch, P of each bacterium; H. cetorum is fusiform, it was only slightly helical, and pitch could not be measured from the images obtained in this study. It can be approximated by the body length. The H. pylori data shown here are the same as in [49]. The H. suis data correspond to the EW configuration. Adapted from Constantino [59].