Sessile bacterium unlocks ability of surface motility through mutualistic interspecies interaction

Abstract

In addition to their common planktonic lifestyle, bacteria frequently live in surface-associated habitats. Surface motility is essential for exploring these habitats for food sources. However, many bacteria are found on surfaces, even though they lack features required for migrating along surfaces. How these canonical non-motile bacteria adapt to the environmental fluctuations on surfaces remains unknown. Recently, several cases of interspecies interaction were reported that induce surface motility of non-motile bacteria either by using hitchhiking strategies or through social spreading mechanisms. Here, we report a previously unknown mechanism for interaction-dependent surface motility of the canonical non-motile bacterium, Dietzia sp. DQ12-45-1b, which is induced by interaction with a dimorphic prosthecate bacterium, Glycocaulis alkaliphilus 6B-8T. Dietzia cells exhibits "sliding"-like motility in an area where the strain Glycocaulis cells was pre-colonized with a sufficient density. Furthermore, we show that biosurfactants play a critical role in inducing the surface motility of Dietzia cells. Our analysis also demonstrates that Dietzia degrade n-alkanes and provide Glycocaulis with the resulting metabolites for survival, which in turn enabled directional migration of Dietzia towards nutrients in the environment. Such interaction-dependent migration was also found between Dietzia and Glycocaulis strains isolated from other habitats, suggesting that this mutualistic relationship ubiquitously occurs in natural environments. In conclusion, we propose a novel model for such a win-win strategy, whereby non-motile bacteria pay metabolites to dimorphic prosthecate bacteria in return for migrating to reach environments otherwise inaccessible. We propose that this mechanism represents a common strategy for canonically non-motile bacteria living on a surface. ImportanceCell motility provides a selective advantage for bacteria searching for nutrients. While a large body of evidence exists for how motile bacteria migrate on surface by virtue of different ways of motility, fewer studies concerned about how canonical non-motile bacteria adapted to those surface-associated habitats. Recent reports have proposed that interactions with other bacteria trigger the movement of those sessile bacteria. However, these interactions are limited to hitchhiking or social spreading modes. Here, we characterized a previously unknown interaction mode between Dietzia and Glycocaulis. This interaction differs from previously described modes, thus advance our limited understanding of how sessile bacteria move on surfaces. We propose that this interaction mode represents a win-win strategy for both strains, and this mode might be widely distributed across diverse environments. These novel insights should greatly assist in understanding the mechanisms responsible for the cellular interplay between microbes in complex microbiomes.