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.

Significance: The resource landscape for marine microbes is composed of microscale resource patches, but whether this microheterogeneity can drive the ecological differentiation of natural microbial populations remains unclear. The tradeoff between two nascent populations of marine bacteria demonstrated here is significant for several reasons. First, it illustrates that principles of spatial ecology, so far only illustrated for animals and plants, apply to the ephemeral, microscale nutrient landscape of marine microbes. Second, the results suggest that differential behavior can ensure coexistence of otherwise very similar populations of organisms. Finally, because the demonstrated tradeoff induces microgeographic separation among the populations, it may be a crucial step in initiating gene flow barriers that ultimately allow the populations to embark on differential evolutionary trajectories.

We describe an innovative experimental and computational approach to control the expression of a protein in a population of yeast cells. We designed a simple control algorithm to automatically regulate the administration of inducer molecules to the cells by comparing the actual protein expression level in the cell population with the desired expression level. We then built an automated platform based on a microfluidic device, a time-lapse microscopy apparatus, and a set of motorized syringes, all controlled by a computer. We tested the platform to force yeast cells to express a desired fixed, or time-varying, amount of a reporter protein over thousands of minutes. The computer automatically switched the type of sugar administered to the cells, its concentration and its duration, according to the control algorithm. Our approach can be used to control expression of any protein, fused to a fluorescent reporter, provided that an external molecule known to (indirectly) affect its promoter activity is available. A crucial feature of biological systems is their ability to maintain homeostasis in spite of ever-changing conditions. In engineering, this ability can be embedded in devices ranging from the thermostat to the autopilot of a modern plane using control systems which operate via a negative feedback mechanism: the quantity to be controlled is measured then subtracted from the desired reference value, and the resulting error is used to compute the control action to be implemented on the physical system (e.g. switching on or off the heating, changing the position of the rudder). Here, we developed and applied a method to regulate the expression level of a protein, in a growing population of cells over several generations, in a completely automatic fashion. We designed and implemented an integrated platform comprising a microfluidic device, a time-lapse microscopy apparatus, and a set of motorized syringes, all controlled by a computer. We tested the platform to force yeast cells to express a desired time-varying amount of a gene in yeast. Our method can be applied to control a protein of interest in vivo allowing to probe the function of biological systems in unprecedented ways.

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.