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Marine bacteria influence Earth's environmental dynamics in fundamental ways by controlling the biogeochemistry and productivity of the oceans. These large-scale consequences result from the combined effect of countless interactions occurring at the level of the individual cells. At these small scales, the ocean is surprisingly heterogeneous, and microbes experience an environment of pervasive and dynamic chemical and physical gradients. Many species actively exploit this heterogeneity, while others rely on gradient-independent adaptations. This is an exciting time to explore this frontier of oceanography, but understanding microbial behavior and competition in the context of the water column's microarchitecture calls for new ecological frameworks, such as a microbial optimal foraging theory, to determine the relevant trade-offs and global consequences of microbial life in a sea of gradients.

How bacterial chemotaxis is performed is much better understood than why. Traditionally, chemotaxis has been understood as a foraging strategy by which bacteria enhance their uptake of nutrients and energy, yet it has remained puzzling why certain less nutritious compounds are strong chemoattractants and vice versa. Recently, we have gained increased understanding of alternative ecological roles of chemotaxis, such as navigational guidance in colony expansion, localization of hosts or symbiotic partners and contribution to microbial diversity by the generation of spatial segregation in bacterial communities. Although bacterial chemotaxis has been observed in a wide range of environmental settings, insights into the phenomenon are mostly based on laboratory studies of model organisms. In this Review, we highlight how observing individual and collective migratory behaviour of bacteria in different settings informs the quantification of trade-offs, including between chemotaxis and growth. We argue that systematically mapping when and where bacteria are motile, in particular by transgenerational bacterial tracking in dynamic environments and in situ approaches from guts to oceans, will open the door to understanding the rich interplay between metabolism and growth and the contribution of chemotaxis to microbial life.Chemotaxis is one of the best studied bacterial behaviours, but the underlying mechanisms are much better understood than the reasons and consequences of chemotaxis. In this Review, Keegstra et al. discuss the costs and benefits both for individual bacteria and whole populations.

Bacteria often reside in fluids. Now, it is shown that hydrodynamic shear, which creates forces and torques on bacterial suspensions, stimulates the attachment of bacteria to surfaces and seriously hinders chemotaxis. Bacteria often live in dynamic fluid environments 1 , 2 , 3 and flow can affect fundamental microbial processes such as nutrient uptake 1 , 4 and infection 5 . However, little is known about the consequences of the forces and torques associated with fluid flow on bacteria. Through microfluidic experiments, we show that fluid shear produces strong spatial heterogeneity in suspensions of motile bacteria, characterized by up to 70% cell depletion from low-shear regions due to ‘trapping’ in high-shear regions. Two mathematical models and a scaling analysis accurately capture these observations, including the maximal depletion at mean shear rates of 2.5–10 s −1 , and reveal that trapping by shear originates from the competition between the cell alignment with the flow and the stochasticity in the swimming orientation. We show that this shear-induced trapping directly impacts widespread bacterial behaviours, by hampering chemotaxis and promoting surface attachment. These results suggest that the hydrodynamic environment may directly affect bacterial fitness and should be carefully considered in the study of microbial processes.

Buckling is often regarding as a form of mechanical failure to be avoided. High-speed video microscopy and mechanical stability theory now show, however, that bacteria use such processes to their advantage. Cells propelled with a single flagellum change direction with a flick-like motion that exploits a buckling instability. Bacteria swim by rotating rigid helical flagella and periodically reorienting to follow environmental cues 1 , 2 . Despite the crucial role of reorientations, their underlying mechanism has remained unknown for most uni-flagellated bacteria 3 , 4 . Here, we report that uni-flagellated bacteria turn by exploiting a finely tuned buckling instability of their hook, the 100-nm-long structure at the base of their flagellar filament 5 . Combining high-speed video microscopy and mechanical stability theory, we demonstrate that reorientations occur 10 ms after the onset of forward swimming, when the hook undergoes compression, and that the associated hydrodynamic load triggers the buckling of the hook. Reducing the load on the hook below the buckling threshold by decreasing the swimming speed results in the suppression of reorientations, consistent with the critical nature of buckling. The mechanism of turning by buckling represents one of the smallest examples in nature of a biological function stemming from controlled mechanical failure 6 and reveals a new role for flexibility in biological materials, which may inspire new microrobotic solutions in medicine and engineering 7 .

Many symbiotic relationships rely on the acquisition of microbial partners from the environment. However, the mechanisms by which microbial symbionts find and colonize their hosts are often unknown. We propose that the acquisition of environmental symbionts often necessitates active migration and colonization by the symbionts through motility and chemotaxis. The pivotal role of these behaviours in the onset and maintenance of symbiotic interactions is well established in a small number of model systems but remains largely overlooked for the many symbioses that involve the recruitment of microbial partners from the environment. In this Review, we highlight when, where and how chemotaxis and motility can enable symbiont recruitment and propose that these symbiont behaviours are important across a wide range of hosts and environments.Many symbioses depend on the acquisition of microbial symbionts from the environment. In this Review, Raina and colleagues argue that chemotaxis and motility are widespread but overlooked mechanisms that enable symbionts to find and/or colonize their hosts.

It has long been known that bacteria coordinate their physiology with their nutrient environment, yet our current understanding offers little intuition for how bacteria respond to the second-to-minute scale fluctuations in nutrient concentration characteristic of many microbial habitats. To investigate the effects of rapid nutrient fluctuations on bacterial growth, we couple custom microfluidics with single-cell microscopy to quantify the growth rate of E. coli experiencing 30 s to 60 min nutrient fluctuations. Compared to steady environments of equal average concentration, fluctuating environments reduce growth rate by up to 50%. However, measured reductions in growth rate are only 38% of the growth loss predicted from single nutrient shifts. This enhancement derives from the distinct growth response of cells grown in environments that fluctuate rather than shift once. We report an unexpected physiology adapted for growth in nutrient fluctuations and implicate nutrient timescale as a critical environmental parameter beyond nutrient identity and concentration. Here the authors use microfluidics and single-cell microscopy to quantify the growth dynamics of individual E. coli cells exposed to nutrient fluctuations with periods as short as 30 seconds, finding that nutrient fluctuations reduce growth rates up to 50% compared to a steady nutrient delivery of equal average concentration, implying that temporal variability is an important parameter in bacterial growth.

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.

The microenvironment surrounding individual phytoplankton cells is often rich in dissolved organic matter (DOM), which can attract bacteria by chemotaxis. These “phycospheres” may be prominent sources of resource heterogeneity in the ocean, affecting the growth of bacterial populations and the fate of DOM. However, these effects remain poorly quantified due to a lack of quantitative ecological frameworks. Here, we used video microscopy to dissect with unprecedented resolution the chemotactic accumulation of marine bacteria around individual Chaetoceros affinis diatoms undergoing lysis. The observed spatiotemporal distribution of bacteria was used in a resource utilization model to map the conditions under which competition between different bacterial groups favors chemotaxis. The model predicts that chemotactic, copiotrophic populations outcompete nonmotile, oligotrophic populations during diatom blooms and bloom collapse conditions, resulting in an increase in the ratio of motile to nonmotile cells and in the succession of populations. Partitioning of DOM between the two populations is strongly dependent on the overall concentration of bacteria and the diffusivity of different DOM substances, and within each population, the growth benefit from phycospheres is experienced by only a small fraction of cells. By informing a DOM utilization model with highly resolved behavioral data, the hybrid approach used here represents a new path toward the elusive goal of predicting the consequences of microscale interactions in the ocean.

The colonization of surfaces by bacteria is a widespread phenomenon with consequences on environmental processes and human health. While much is known about the molecular mechanisms of surface colonization, the influence of the physical environment remains poorly understood. Here we show that the colonization of non-planar surfaces by motile bacteria is largely controlled by flow. Using microfluidic experiments with Pseudomonas aeruginosa and Escherichia coli , we demonstrate that the velocity gradients created by a curved surface drive preferential attachment to specific regions of the collecting surface, namely the leeward side of cylinders and immediately downstream of apexes on corrugated surfaces, in stark contrast to where nonmotile cells attach. Attachment location and rate depend on the local hydrodynamics and, as revealed by a mathematical model benchmarked on the observations, on cell morphology and swimming traits. These results highlight the importance of flow on the magnitude and location of bacterial colonization of surfaces. Bacterial colonization of surfaces has a profound environmental, technological and medical impact. Here, Secchi et al. show how fluid flow affects the magnitude and location of bacterial colonization on curved surfaces through its coupling with cell morphology and motility.