Surfing Motility: a Conserved yet Diverse Adaptation among Motile Bacteria

Abstract

Bacterial rapid surfing motility is a novel surface adaptation of <i>Pseudomonas aeruginosa</i> in the presence of the glycoprotein mucin. Here, we show that other Gram-negative motile bacterial species, including <i>Escherichia coli</i>, <i>Salmonella enterica</i>, <i>Vibrio harveyi</i>, <i>Enterobacter cloacae</i>, and <i>Proteus mirabilis</i>, also exhibit the physical characteristics of surfing on the surface of agar plates containing 0.4% mucin, where surfing motility was generally more rapid and less dependent on medium viscosity than was swimming motility. As previously observed in <i>Pseudomonas aeruginosa</i>, all surfing species exhibited some level of broad-spectrum adaptive resistance, although the antibiotics to which they demonstrated surfing-mediated resistance differed. Surfing motility in <i>P. aeruginosa</i> was found to be dependent on the quorum-sensing systems of this organism; however, this aspect was not conserved in other tested bacterial species, including <i>V. harveyi</i> and <i>S. enterica</i>, as demonstrated by assaying specific quorum-sensing mutants. Thus, rapid surfing motility is a complex surface growth adaptation that is conserved in several motile bacteria, involves flagella, and leads to diverse broad-spectrum antibiotic resistance, but it is distinct in terms of dependence on quorum sensing.<b>IMPORTANCE</b> This study showed for the first time that surfing motility, a novel form of surface motility first discovered in <i>Pseudomonas aeruginosa</i> under artificial cystic fibrosis conditions, including the presence of high mucin content, is conserved in other motile bacterial species known to be mucosa-associated, including <i>Escherichia coli</i>, <i>Salmonella enterica</i>, and <i>Proteus mirabilis</i> Here, we demonstrated that key characteristics of surfing, including the ability to adapt to various viscous environments and multidrug adaptive resistance, are also conserved. Using mutagenesis assays, we also identified the importance of all three known quorum-sensing systems, Las, Rhl, and Pqs, in <i>P. aeruginosa</i> in regulating surfing motility, and we also observed a conserved dependence of surfing on flagella in certain species.