Marine Microbes See a Sea of Gradients Stocker, Roman
Science (American Association for the Advancement of Science),
11/2012, Letnik:
338, Številka:
6107
Journal Article
Recenzirano
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.
Despite numerous surveys of gene and species content in heterotrophic microbial communities, such as those found in animal guts, oceans, or soils, it is still unclear whether there are generalizable ...biological or ecological processes that control their dynamics and function. Here, we review experimental and theoretical advances to argue that networks of trophic interactions, in which the metabolic excretions of one species are the primary resource for another, constitute the central drivers of microbial community assembly. Trophic interactions emerge from the deconstruction of complex forms of organic matter into a wealth of smaller metabolic intermediates, some of which are released to the environment and serve as a nutritional buffet for the community. The structure of the emergent trophic network and the rate at which primary resources are supplied control many features of microbial community assembly, including the relative contributions of competition and cooperation and the emergence of alternative community states. Viewing microbial community assembly through the lens of trophic interactions also has important implications for the spatial dynamics of communities as well as the functional redundancy of taxonomic groups. Given the ubiquity of trophic interactions across environments, they impart a common logic that can enable the development of a more quantitative and predictive microbial community ecology.
What are the principles that underlie the assembly and succession of dynamic and complex microbial communities? In this Review, Gralka et al. lay out a conceptual framework to understand this issue, arguing that networks of trophic interactions constitute the central drivers of microbial community assembly.
Bacteria often live in dynamic fluid environments and flow can affect fundamental microbial processes such as nutrient uptake and infection. 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 super(-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.
Microfluidics has significantly contributed to the expansion of the frontiers of microbial ecology over the past decade by allowing researchers to observe the behaviors of microbes in highly ...controlled microenvironments, across scales from a single cell to mixed communities. Spatially and temporally varying distributions of organisms and chemical cues that mimic natural microbial habitats can now be established by exploiting physics at the micrometer scale and by incorporating structures with specific geometries and materials. In this article, we review applications of microfluidics that have resulted in insightful discoveries on fundamental aspects of microbial life, ranging from growth and sensing to cell-cell interactions and population dynamics. We anticipate that this flexible multidisciplinary technology will continue to facilitate discoveries regarding the ecology of microorganisms and help uncover strategies to control microbial processes such as biofilm formation and antibiotic resistance.
Bacteria swim by rotating rigid helical flagella and periodically reorienting to follow environmental cues. Despite the crucial role of reorientations, their underlying mechanism has remained unknown ...for most uni-flagellated bacteria. 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. 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 and reveals a new role for flexibility in biological materials, which may inspire new microrobotic solutions in medicine and engineering. PUBLICATION ABSTRACT
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.
Bacteria play an indispensable role in marine biogeochemistry by recycling dissolved organic matter. Motile species can exploit small, ephemeral solute patches through chemotaxis and thereby gain a ...fitness advantage over nonmotile competitors. This competition occurs in a turbulent environment yet turbulence is generally considered inconsequential for bacterial uptake. In contrast, we show that turbulence affects uptake by stirring nutrient patches into networks of thin filaments that motile bacteria can readily exploit. We find that chemotactic motility is subject to a trade-off between the uptake benefit due to chemotaxis and the cost of locomotion, resulting in an optimal swimming speed. A second trade-off results from the competing effects of stirring and mixing and leads to the prediction that chemotaxis is optimally favored at intermediate turbulence intensities.
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.
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