Wall entrapment enhances bacterial chemotactic response to deposited aerosols in the microlayer
The sea surface microlayer is the thin layer of water separating the atmosphere from marine waters below. This typically half-millimeter-deep laminar layer mediates all gas exchange and receives all material deposited from the atmosphere, such as aerosol particles, before any transfer to deeper water can occur. The microlayer is a harsh environment characterized by large temperature and salinity fluctuations and strong ultraviolet radiation. Yet field sampling suggests a microlayer bacterial community does indeed exist, distinct from that in deeper waters. We hypothesize that motile microlayer and near-surface bacteria can successfully exploit the transient nutrient patches produced by surface-deposited aerosols using chemotaxis-driven foraging strategies, thus obtaining privileged access to rare resources. We developed a novel millifluidic device to image a static air-water interface with falling aerosol particles and swimming bacteria, enabling tracking of individual particles and cells. We observed that marine bacteria swam to and accumulated at the surface when exposed to environmentally relevant fluxes of deposited chemoattractant aerosols. These accumulations formed within seconds to minutes in extraordinarily thin films (< 0.1 mm) and were approximately an order of magnitude higher than expected from previously established chemotactic accumulations observed in bulk. Using a novel theoretical model of bacterial behavior, we demonstrated that this strong accumulation can indeed be explained by the coupling of chemotaxis to dissolved aerosol-borne attractants and ‘wall entrapment’ at the air-water interface – a physical mechanism by which motile bacteria reside near boundaries for longer times. Our results highlight how interfaces in the environment modify the behavior of microorganisms, and in particular demonstrate that the microlayer is an environment where motile bacteria, through both active and passive mechanisms, quickly respond to aerosol deposition and accumulate in high-nutrient regions, thus resulting in a competitive advantage for motile cells.