Structure, gene regulation and environmental response of flagella in Vibrio

Abstract

Vibrio species are Gram-negative, rod-shaped bacteria that live in aqueous environments. Several species, such as V. harveyi, V. alginotyticus, and V. splendidus, are associated with diseases in fish or shellfish. In addition, a few species, such as V. cholerae and V. parahaemolyticus, are risky for humans due to infections from eating raw shellfish infected with these bacteria or from exposure of wounds to the marine environment. Bacterial flagella are not essential to live in a culture medium. However, most Vibrio species are motile and have rotating flagella which allow them to move into favorable environments or to escape from unfavorable environments. This review summarizes recent studies about the flagellar structure, function, and regulation of Vibrio species, especially focused on the Na(+)-driven polar flagella that are principally responsible for motility and sensing the surrounding environment, and discusses the relationship between flagella and pathogenicity.

Keywords: bacterial flagellum; chemotaxis; ion-driven motor; motility; pathogenicity.

Figure 1

Flagellar structure of Vibrio. (A) Polar flagellum and lateral flagella in some Vibrio species (not including Vibrio cholerae). (B) Schematic diagram of the hook basal body for a polar flagellum shown in the left half (based on EM images, (Terashima et al., 2006, 2013)) and the lateral flagellar structure shown in the right half, according to the peritrichous flagellum from Salmonella (MacNab, 2003). The characteristics of the polar flagellum are the H ring and the T ring, shown in red.

Figure 2

Model for the basal body ring formation of the Na⁺-driven polar flagellum. The H ring is constructed dependent on FlgT proteins that assemble around the previously formed L ring and P ring. Next, MotX and MotY assemble around the basal body to stably form the T ring with the help of the middle domain of FlgT. As a result, the stator is incorporated properly and works in the presence of the T ring. The model is drawn based on a previous report (Terashima et al., 2013).

Figure 3

Plausible hierarchy of polar flagellum gene expression in Vibrio, based on previous reports (McCarter, ; Correa et al., ; Kojima et al., 2011). The arrows indicate the transcription unit and the number at the beginning of arrow indicates the class of transcriptional hierarchy.

Figure 4

Model for regulation of the number of polar flagella in Vibrio. The function of FlhF is probably inhibited by an interaction with FlhG, a negative regulator of FlhF, and thereby the number of polar flagellum is limited to one. The schemes are drawn based on a previous report (Kusumoto et al., 2008).

Figure 5

Simplified scheme of the chemotaxis signal transduction cascade in Vibrio species. The scheme is drawn based on a previous report (Boin et al., 2004).

Figure 6

Relationship between the motility of the polar flagellum of Vibrio and pathogenicity. (A) In an intestinal environment, because of the presence of bile, the gene expression of virulence is “OFF.” When the polar flagellum senses the high viscosity of the mucus gel, the motility is blocked, lateral flagella or pili are induced, and pathogenic gene expression, including toxins (black solid dots) is kept “ON” presumably because of the reduced bile concentration. (B) In an extra-intestinal environment, c-di-GMP (solid black dots) facilitates Vibrio from the motile-to-sessile transition by decreasing migration due to the binding of the YcgR homolog to the flagellar motor, which causes a reduction of motility and induces the biofilm formation and the suppression on the motility by releasing a lots of polysaccharides. The schemes are drawn based on previous reports (Krasteva et al., ; Boyd and O'Toole, 2012).