Kwangmin Son

A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals.

Diseases are an emerging threat to ocean ecosystems. Coral reefs, in particular, are experiencing a worldwide decline because of disease and bleaching, which have been exacerbated by rising seawater temperatures. Yet, the ecological mechanisms behind most coral diseases remain unidentified. Here, we demonstrate that a coral pathogen, Vibrio coralliilyticus, uses chemotaxis and chemokinesis to target the mucus of its coral host, Pocillopora damicornis. A primary driver of this response is the host metabolite dimethylsulfoniopropionate (DMSP), a key element in the global sulfur cycle and a potent foraging cue throughout the marine food web. Coral mucus is rich in DMSP, and we found that DMSP alone elicits chemotactic responses of comparable intensity to whole mucus. Furthermore, in heat-stressed coral fragments, DMSP concentrations increased fivefold and the pathogen’s chemotactic response was correspondingly enhanced. Intriguingly, despite being a rich source of carbon and sulfur, DMSP is not metabolized by the pathogen, suggesting that it is used purely as an infochemical for host location. These results reveal a new role for DMSP in coral disease, demonstrate the importance of chemical signaling and swimming behavior in the recruitment of pathogens to corals and highlight the impact of increased seawater temperatures on disease pathways.

Live from under the lens: exploring microbial motility with dynamic imaging and microfluidics

Motility is one of the most dynamic features of the microbial world. The ability to swim or crawl frequently governs how microorganisms interact with their physical and chemical environments, and underpins a myriad of microbial processes. The ability to resolve temporal dynamics through time-lapse video microscopy and the precise control of the physicochemical microenvironment afforded by microfluidics offer powerful new opportunities to study the many motility adaptations of microorganisms and thereby further our understanding of their ecology. In this Review, we outline recent insights into the motility strategies of microorganisms brought about by these techniques, including the hydrodynamic signature of microorganisms, their locomotion mechanics, chemotaxis, their motility near and on surfaces, swimming in moving fluids and motility in dense microbial suspensions.

Temperature-induced behavioral switches in a bacterial coral pathogen

Evidence to date indicates that elevated seawater temperatures increase the occurrence of coral disease, which is frequently microbial in origin. Microbial behaviors such as motility and chemotaxis are often implicated in coral colonization and infection, yet little is known about the effect of warming temperatures on these behaviors. Here we present data demonstrating that increasing water temperatures induce two behavioral switches in the coral pathogen Vibrio coralliilyticus that considerably augment the bacterium’s performance in tracking the chemical signals of its coral host, Pocillopora damicornis. Coupling field-based heat-stress manipulations with laboratory-based observations in microfluidic devices, we recorded the swimming behavior of thousands of individual pathogen cells at different temperatures, associated with current and future climate scenarios. When temperature reached ⩾23 °C, we found that the pathogen’s chemotactic ability toward coral mucus increased by >60%, denoting an enhanced capability to track host-derived chemical cues. Raising the temperature further, to 30 °C, increased the pathogen’s chemokinetic ability by >57%, denoting an enhanced capability of cells to accelerate in favorable, mucus-rich chemical conditions. This work demonstrates that increasing temperature can have strong, multifarious effects that enhance the motile behaviors and host-seeking efficiency of a marine bacterial pathogen.

Speed-dependent chemotactic precision in marine bacteria

Significance Our understanding of bacterial chemotaxis, a fundamental nutrient-seeking strategy in the microbial world, mainly derives from Escherichia coli. However, it has become clear that marine bacteria evolved fundamentally different chemotaxis adaptations, often allowing them to accumulate at resource peaks more tightly and rapidly than E. coli. We studied the origin of this high chemotactic precision and found that it lies in an unexpected dependence of chemotaxis on swimming speed: faster cells have substantially higher precision, counter to all known models of chemotaxis. We elucidate this finding through a combination of single-cell tracking of thousands of marine bacteria in microfluidic gradients and a mathematical model of chemotaxis that explicitly accounts for swimming speed in the chemotaxis pathway. Chemotaxis underpins important ecological processes in marine bacteria, from the association with primary producers to the colonization of particles and hosts. Marine bacteria often swim with a single flagellum at high speeds, alternating “runs” with either 180° reversals or ∼90° “flicks,” the latter resulting from a buckling instability of the flagellum. These adaptations diverge from Escherichia coli’s classic run-and-tumble motility, yet how they relate to the strong and rapid chemotaxis characteristic of marine bacteria has remained unknown. We investigated the relationship between swimming speed, run–reverse–flick motility, and high-performance chemotaxis by tracking thousands of Vibrio alginolyticus cells in microfluidic gradients. At odds with current chemotaxis models, we found that chemotactic precision—the strength of accumulation of cells at the peak of a gradient—is swimming-speed dependent in V. alginolyticus. Faster cells accumulate twofold more tightly by chemotaxis compared with slower cells, attaining an advantage in the exploitation of a resource additional to that of faster gradient climbing. Trajectory analysis and an agent-based mathematical model revealed that this unexpected advantage originates from a speed dependence of reorientation frequency and flicking, which were higher for faster cells, and was compounded by chemokinesis, an increase in speed with resource concentration. The absence of any one of these adaptations led to a 65–70% reduction in the population-level resource exposure. These findings indicate that, contrary to what occurs in E. coli, swimming speed can be a fundamental determinant of the gradient-seeking capabilities of marine bacteria, and suggest a new model of bacterial chemotaxis.

Flagella, flexibility and flow: Physical processes in microbial ecology

How microorganisms interact with their environment and with their conspecifics depends strongly on their mechanical properties, on the hydrodynamic signatures they generate while swimming and on fluid flows in their environment. The rich fluid-structure interaction between flagella – the appendages microorganisms use for propulsion – and the surrounding flow, has broad reaching effects for both eukaryotic and prokaryotic microorganisms. Here, we discuss selected recent advances in our understanding of the physical ecology of microorganisms, which have hinged on the ability to directly interrogate the movement of individual cells and their swimming appendages, in precisely controlled fluid environments, and to image them at appropriately fast timescales. We review how a flagellar buckling instability can unexpectedly serve a fundamental function in the motility of bacteria, we elucidate the role of hydrodynamics and flexibility in the emergent properties of groups of eukaryotic flagella, and we show how fluid flows characteristic of microbial habitats can strongly bias the migration and spatial distribution of bacteria. The topics covered here are illustrative of the potential inherent in the adoption of experimental methods and conceptual frameworks from physics in understanding the lives of microorganisms.