Remodeling of Chemotaxis is a Cornerstone of Bacterial Swarming

Abstract

21Many bacteria use flagella-driven motility to swarm or move collectively over a surface terrain. 22 Bacterial adaptations for swarming can include cell elongation, hyper-flagellation, recruitment of 23 special stator proteins and surfactant secretion, among others. We recently demonstrated another 24 swarming adaptation in Escherichia coli, wherein the chemotaxis pathway is remodeled to increase 25 run durations (decrease tumble bias), with running speeds increased as well. We show here that 26 the modification of motility parameters during swarming is not unique to E. coli, but shared by a 27 diverse group of bacteria we examined -Proteus mirabilis, Serratia marcescens, Salmonella 28 enterica, Bacillus subtilis, and Pseudomonas aeruginosa -suggesting that altering the 29 chemosensory physiology is a cornerstone of swarming. 30 31 32 33 34 35 36 37 38 39 40 41 42 Importance 43 Bacteria within a swarm move characteristically in packs, displaying an intricate swirling motion 44 where hundreds of dynamic packs continuously form and dissociate as the swarm colonizes 45 increasing expanse of territory. The demonstrated property of E. coli to reduce its tumble bias and 46 hence increase its run duration during swarming is expected to maintain/promote side-by-side 47 alignment and cohesion within the bacterial packs. Here we observe a similar low tumble bias in 48 five different bacterial species, both Gram positive and Gram negative, each inhabiting a unique 49 habitat and posing unique problems to our health. The unanimous display of an altered run-tumble 50 bias in swarms of all species examined here suggests that this behavioral adaptation is crucial for 51 swarming.52 53 54 55 56 57 58 59 60 61 62 63 65 flagella (1-3). A wide array of phenotypic adaptations are associated with swarming. A common 66 attribute of all swarms is a pattern of ceaseless circling motion, in which packs of cells all traveling 67 in the same directions split and merge, with continuous exchange of bacteria between the packs 68 (3-5). This behavior differs from movement of the bacteria in bulk liquid, where they swim 69 individually (6). In E. coli, the mechanics of flagella are similar during both swimming and 70 swarming in that peritrichous flagella driven by bi-directional rotary motors switch between 71 counterclockwise (CCW) and clockwise (CW) directions. However, while CCW rotation promotes 72 formation of a coherent flagellar bundle that propels the cell forward (run) during both swimming 73 and swarming, a transient switch in rotational direction (CW) causes the cell to tumble while 74swimming, but reverse direction while swarming (7,8). 75The switching frequency of the flagellar motor is controlled by the chemotaxis system, best 76 studied in E. coli, where transmembrane receptors detect extracellular signals and transmit them 77 via phosphorelay to the motor, to promote migration to favorable locales during swimming (9). 78The ability to perform chemotaxis is not essential for swarming, but a basal tumble bias is 79 important ...