Viscosity-dependent variations in the cell shape and swimming manner of Leptospira

Abstract

Spirochaetes are spiral or flat-wave-shaped Gram-negative bacteria that have periplasmic flagella between the peptidoglycan layer and outer membrane. Rotation of the periplasmic flagella transforms the cell body shape periodically, allowing the cell to swim in aqueous environments. Because the virulence of motility-deficient mutants of pathogenic species is drastically attenuated, motility is thought to be an essential virulence factor in spirochaetes. However, it remains unknown how motility practically contributes to the infection process. We show here that the cell body configuration and motility of the zoonotic spirochaete Leptospira changes depending on the viscosity of the medium. Leptospira swim and reverse the swimming direction by transforming the cell body. Motility analysis showed that the frequency of cell shape transformation was increased by increasing the viscosity of the medium. The increased cell body transformation induced highly frequent reversal of the swimming direction. A simple kinetic model based on the experimental results shows that the viscosity-induced increase in reversal limits cell migration, resulting in the accumulation of cells in high-viscosity regions. This behaviour could facilitate the colonization of the spirochaete on host tissues covered with mucosa.

Protein expression in the obligate hydrocarbon‐degrading psychrophile Oleispira antarctica RB‐8 during alkane degradation and cold tolerance

“…The main cause to increase the flagella switching frequency (CCW to CW) is the chemotaxis signalling pathway, and several components of this pathway showed increased biosynthesis at 4°C. In the pathway, stimulation of the chemotaxis receptors, also known as MCPs, is followed by phosphorylation or acetylation of the response regulator CheY; phosphorylated (CheY‐P) or acetylated (CheY‐Asc); CheY then associates with the rotor of the flagella motor, and the motor changes direction to CW (Porter et al ., ; Takabe et al ., ). Six MCPs showed increased biosynthesis (Fig.…”

Implications of back-and-forth motion and powerful propulsion for spirochetal invasion

“…Enhancement of swimming reversal has been observed in polymer solutions, where the entire spirochetal body was exposed to changes in environmental viscosity or viscoelasticity 12 . However, we showed that swimming reversal is increased by that very limited part of the cell body is placed in viscoelastic milieu.…”

“…1B), and the morphology of the cell ends changes between spiral and hook shapes frequently: An asymmetric configuration showing spiral and hook shapes at the anterior and posterior cell ends, respectively, propels the cell unidirectionally ( Fig. 1B) [10][11][12][13] . As with other motile species, the motility of Leptospira spp.…”

“…are closely related to their pathogenicity 14,15 , but how it practically works as a virulence factor in the spirochete remains unclear. As a possible scenario for the motility dependence of the Leptospira pathogenicity, we recently showed that the spirochete increased the frequency of changing the swimming direction with the elevated viscosity of polymer solutions, and the resultant limitation of their net migrations could be involved in accumulation of the spirochete in epithelial mucosa in vivo 12 . In this study, hypothesizing the significance of the phenomenon observed in polymer solution for percutaneous infection of Leptospira, we investigated their behaviors at the border of liquid and gel phases resembling the skin dermis exposed to the contaminated environmental water.…”

Spirochete Flagella and Motility

“…is distinguished from the other two spirochetes by a small cell width and short wavelength [4,10]. The protoplasmic cylinder of Leptospira (Figure 1b and c) is relatively rigid, maintaining the helix parameters even during swimming, whereas both ends of the cell body are frequently transformed, as described later [11][12][13][14]. Unlike Borrelia and Brachyspira, PFs of Leptospira are too short to overlap [15].…”