Interspecies surfactants serve as public goods enabling surface motility in Pseudomonas aeruginosa.

Abstract

In most natural environments, bacteria live in polymicrobial communities where secreted molecules from neighboring species alter bacterial behaviors, including motility, but such interactions are understudied. Pseudomonas aeruginosa is a motile opportunistic pathogen that exists in diverse multispecies environments, such as the soil, and is frequently found in human wound and respiratory tract co-infections with other bacteria, including Staphylococcus aureus. Here, we show that P. aeruginosa can co-opt secreted surfactants from other species for flagellar-based surface motility. We found that exogenous surfactants from S. aureus, other bacteria, and interkingdom species enabled P. aeruginosa to switch from swarming to an alternative surface spreading motility on semi-solid surfaces and allowed for the emergence of surface motility on hard agar where P. aeruginosa was otherwise unable to move. Although active flagellar function was required for surface spreading, known motility regulators were not essential, indicating that surface spreading may be regulated by an as yet unknown mechanism. This motility was distinct from the response of most other motile bacterial species in the presence of exogenous surfactants. Mutant analysis indicated that this P. aeruginosa motility was similar to a previously described mucin-based motility, "surfing," albeit with divergent regulation. Thus, our study demonstrates that secreted surfactants from the host as well as neighboring bacterial and interkingdom species act as public goods facilitating P. aeruginosa flagella-mediated surfing-like surface motility, thereby allowing it to access different environmental niches.

Importance: Bacterial motility is an important determinant of bacterial fitness and pathogenesis, allowing expansion and invasion to access nutrients and adapt to new environments. Here, we demonstrate that secreted surfactants from a variety of foreign species, including other bacterial species, infection hosts, fungi, and plants, facilitate surface spreading motility in the opportunistic pathogen Pseudomonas aeruginosa that is distinct from established motility phenotypes. This response to foreign surfactants also occurs in Pseudomonas putida, but not in more distantly related bacterial species. Our systematic characterization of surfactant-based surface spreading shows that these interspecies surfactants serve as public goods to enable P. aeruginosa to move and explore environmental conditions when it would be otherwise immotile.