Abstract
The γ-proteobacteria are a group of diverse bacteria including pathogenic Escherichia, Salmonella, Vibrio, and Pseudomonas species. The majority swim in liquids with polar, sodium-driven flagella and swarm on surfaces with lateral, non-chemotactic flagella. Notable exceptions are the enteric Enterobacteriaceae such as Salmonella and E. coli. Many of the well-studied Enterobacteriaceae are gut bacteria that both swim and swarm with the same proton-driven peritrichous flagella. How different flagella evolved in closely related lineages, however, has remained unclear. Here, we describe our phylogenetic finding that Enterobacteriaceae flagella are not native polar or lateral γ-proteobacterial flagella but were horizontally acquired from an ancestral β-proteobacterium. Using electron cryo-tomography and subtomogram averaging, we confirmed that Enterobacteriaceae flagellar motors resemble contemporary β-proteobacterial motors and are distinct to the polar and lateral motors of other γ-proteobacteria. Structural comparisons support a model in which γ-proteobacterial motors have specialized, suggesting that acquisition of a β-proteobacterial flagellum may have been beneficial as a general-purpose motor suitable for adjusting to diverse conditions. This acquisition may have played a role in the development of the enteric lifestyle.
Highlights
Understanding molecular evolution is fundamental to contemporary biology
To understand the differences between the peritrichous flagella of the enteric γ-proteobacteria and the polar and lateral flagella of other γ-proteobacteria, we determined a flagellar phylogeny across > 90 species manually selected based on relevance and diversity by concatenating the protein sequences of their core flagellar proteins
We found that the polar and lateral γ-proteobacterial motors clustered together, but the peritrichous enteric motor instead branched from within the β-proteobacterial motors, suggesting horizontal acquisition from a member of the β-proteobacteria (Figure 1A), and we focused on a phylogeny of 48 β- and γ-proteobacteria for further inspection (Figures 1B,D and Supplementary Figures S4, S5)
Summary
Understanding molecular evolution is fundamental to contemporary biology. Compared to evolutionary processes in large eukaryotes, relatively little is known about how molecular machines are acquired, adapted, or change function, and how this relates to the environment. Enterics swim with a biased random walk: when all flagella rotate counterclockwise, the universal joints facilitate bundling of flagella for propulsion. Instead of multifunctional peritrichous flagella, nonenteric γ-proteobacteria have high-torque polar motors, usually Na+-driven, with high-occupancy stator complexes held in place by large periplasmic disks (Terashima et al, 2006, 2010; Beeby et al, 2016; Zhu et al, 2017); many γ-proteobacteria have secondary lateral flagella used for surface-based swarming motility, or as “rudders” (Bubendorfer et al, 2014). Phylogenetic and structural results reveal that the enterics acquired a β-proteobacterial flagellar motor by horizontal transfer This transfer may have provided contemporary enteric bacteria with a general-purpose motor better able to adjust its behavior to a wide range of environmental conditions than the more specialized motors native to the γ-proteobacteria
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