Spatial organization in bacterial chemotaxis

Spatial organization of signalling is not an exclusive property of eukaryotic cells. Despite the fact that bacterial signalling pathways are generally simpler than those in eukaryotes, there are several well‐documented examples of higher‐order intracellular signalling structures in bacteria. One of the most prominent and best‐characterized structures is formed by proteins that control bacterial chemotaxis. Signals in chemotaxis are processed by ordered arrays, or clusters, of receptors and associated proteins, which amplify and integrate chemotactic stimuli in a highly cooperative manner. Receptor clusters further serve to scaffold protein interactions, enhancing the efficiency and specificity of the pathway reactions and preventing the formation of signalling gradients through the cell body. Moreover, clustering can also ensure spatial separation of multiple chemotaxis systems in one bacterium. Assembly of receptor clusters appears to be a stochastic process, but bacteria evolved mechanisms to ensure optimal cluster distribution along the cell body for partitioning to daughter cells at division.     

Multiple CheY Homologs Control Swimming Reversals and Transient Pauses in Azospirillum brasilense

Chemotaxis, together with motility, helps bacteria foraging in their habitat. Motile bacteria exhibit a variety of motility patterns, often controlled by chemotaxis, to promote dispersal. Motility in many bacteria is powered by a bidirectional flagellar motor. The flagellar motor has been known to briefly pause during rotation because of incomplete reversals or stator detachment. Transient pauses were previously observed in bacterial strains lacking CheY, and these events could not be explained by incomplete motor reversals or stator detachment. Here, we systematically analyzed swimming trajectories of various chemotaxis mutants of the monotrichous soil bacterium, Azospirillum brasilense. Like other polar flagellated bacterium, the main swimming pattern in A. brasilense is run and reverse. A. brasilense also uses run-pauses and putative run-reverse-flick-like swimming patterns, although these are rare events. A. brasilense mutant derivatives lacking the chemotaxis master histidine kinase, CheA4, or the central response regulator, CheY7, also showed transient pauses. Strikingly, the frequency of transient pauses increased dramatically in the absence of CheY4. Our findings collectively suggest that reversals and pauses are controlled through signaling by distinct CheY homologs, and thus are likely to be functionally important in the lifestyle of this soil organism.     

Bacterial chemotaxis in an optical trap

An optical trapping technique is implemented to investigate the chemotactic behavior of a marine bacterial strain Vibrio alginolyticus. The technique takes the advantage that the bacterium has only a single polar flagellum, which can rotate either in the counter-clock-wise or clock-wise direction. The two rotation states of the motor can be readily and instantaneously resolved in the optical trap, allowing the flagellar motor switching rate S(t) to be measured under different chemical stimulations. In this paper the focus will be on the bacterial response to an impulsive change of chemoattractant serine. Despite different propulsion apparati and motility patterns, cells of V. alginolyticus apparently use a similar response as Escherichia coli to regulate their chemotactic behavior. Specifically, we found that the switching rate S(t) of the bacterial motor exhibits a biphasic behavior, showing a fast initial response followed by a slow relaxation to the steady-state switching rate S0. The measured S(t) can be mimicked by a model that has been recently proposed for chemotaxis in E. coli. The similarity in the response to the brief chemical stimulation in these two different bacteria is striking, suggesting that the biphasic response may be evolutionarily conserved. This study also demonstrated that optical tweezers can be a useful tool for chemotaxis studies and should be applicable to other polarly flagellated bacteria.     

Microcolony and biofilm formation as a survival strategy for bacteria

Bacterial communities such as biofilms are widely recognized as being important for survival and persistence of bacteria in harsh environments. Mechanistic models of biofilm growth indicate that the way in which the surface is seeded can effect the morphology of simulated biofilms. Experimental studies indicate that genes which are important for chemotaxis also influence biofilm formation, perhaps by influencing aggregation on a surface. Understanding aggregation and microcolony formation could therefore help clarify factors influencing biofilm formation and illuminate how groups influence the fitness of bacteria. In this paper I develop an individual based model to examine how different behaviors involved in microcolony formation on a surface determine patterns of group sizes and link patterns to bacterial fitness.     

Bacterial Motility Patterns Reveal Importance of Exploitation over Exploration in Marine Microhabitats. Part I: Theory

Bacteria use different motility patterns to navigate and explore natural habitats. However, how these motility patterns are selected, and what their benefits may be, are not understood. In this article, we analyze the effect of motility patterns on a cell’s ability to migrate in a chemical gradient and to localize at the top of the gradient, the two most important characteristics of bacterial chemotaxis. We will focus on two motility patterns, run-tumble and run-reverse-flick, that are observed and characterized in enteric bacterium Escherichia coli and marine bacterium Vibrio alginolyticus, respectively. To make an objective comparison, master equations are developed on the basis of microscopic motions of the bacteria. An unexpected yet significant result is that by adopting the run-reverse-flick motility pattern, a bacterium can reduce its diffusivity without compromising its drift in the chemical gradient. This finding is biologically important as it suggests that the motility pattern can improve a microorganism’s ability to sequester nutrients in a competitive environment.     

Bacterial Motility Patterns Reveal Importance of Exploitation over Exploration in Marine Microhabitats. Part I: Theory

Bacteria use different motility patterns to navigate and explore natural habitats. However, how these motility patterns are selected, and what their benefits may be, are not understood. In this article, we analyze the effect of motility patterns on a cell’s ability to migrate in a chemical gradient and to localize at the top of the gradient, the two most important characteristics of bacterial chemotaxis. We will focus on two motility patterns, run-tumble and run-reverse-flick, that are observed and characterized in enteric bacterium Escherichia coli and marine bacterium Vibrio alginolyticus, respectively. To make an objective comparison, master equations are developed on the basis of microscopic motions of the bacteria. An unexpected yet significant result is that by adopting the run-reverse-flick motility pattern, a bacterium can reduce its diffusivity without compromising its drift in the chemical gradient. This finding is biologically important as it suggests that the motility pattern can improve a microorganism’s ability to sequester nutrients in a competitive environment.     

Chemotaxis by Naegleria fowleri for bacteria

Naegleria fowleri amebae demonstrated a chemotactic and chemokinetic response toward live cells and extracts of Escherichia coli and other bacterial species when experiments were performed using a blind-well chemotaxis chamber. The peptide N-formyl-methionyl-leucyl-phenylalanine acted as a chemokinetic rather than a chemotactic factor for N. fowleri amebae. Competition experiments in which nerve cell extracts or bacteria were placed on either side of the filter in chemotaxis chambers resulted in increased movement towards bacteria. A scanning electron microscopy study of the interaction of N. fowleri with different bacterial species confirmed that when the amebae were near ingestible bacteria they moved toward the bacteria by pseudopod formation. Naegleria fowleri appeared to respond to bacteria by three interrelated but distinct processes: chemokinesis, chemotaxis, and formation of food cups.     

A minimal model of metabolism-based chemotaxis

Since the pioneering work by Julius Adler in the 1960's, bacterial chemotaxis has been predominantly studied as metabolism-independent. All available simulation models of bacterial chemotaxis endorse this assumption. Recent studies have shown, however, that many metabolism-dependent chemotactic patterns occur in bacteria. We hereby present the simplest artificial protocell model capable of performing metabolism-based chemotaxis. The model serves as a proof of concept to show how even the simplest metabolism can sustain chemotactic patterns of varying sophistication. It also reproduces a set of phenomena that have recently attracted attention on bacterial chemotaxis and provides insights about alternative mechanisms that could instantiate them. We conclude that relaxing the metabolism-independent assumption provides important theoretical advances, forces us to rethink some established pre-conceptions and may help us better understand unexplored and poorly understood aspects of bacterial chemotaxis.     

Chemotactic Sensing towards Ambient and Secreted Attractant Drives Collective Behaviour of E. coli

We simulate the dynamics of a suspension of bacterial swimmers, which chemotactically sense gradients in either ambient or self-secreted attractants (e.g. nutrient or aspartate respectively), or in both. Unlike previous mean field models based on a set of continuum partial differential equations, our model resolves single swimmers and therefore incorporates stochasticity and effects due to fluctuations in the bacterial density field. The algorithm we use is simple enough that we can follow the evolution of colonies of up to over a million bacteria for timescales relevant to pattern formation for E. coli growing in semisolid medium such as agar, or in confined geometries. Our results confirm previous mean field results that the patterns observed experimentally can be reproduced with a model incorporating chemoattractant secretion, chemotaxis (towards gradients in the chemoattractant field), and bacterial reproduction. They also suggest that further experiments with bacterial strains chemotactically moving up both nutrient and secreted attractant field may yield yet more dynamical patterns.     

Residence time calculation for chemotactic bacteria within porous media

Local chemical gradients can have a significant impact on bacterial population distributions within subsurface environments by evoking chemotactic responses. These local gradients may be created by consumption of a slowly diffusing nutrient, generation of a local food source from cell lysis, or dissolution of nonaqueous phase liquids trapped within the interstices of a soil matrix. We used a random walk simulation algorithm to study the effect of a local microscopic gradient on the swimming behavior of bacteria in a porous medium. The model porous medium was constructed using molecular dynamics simulations applied to a fluid of equal-sized spheres. The chemoattractant gradient was approximated with spherical symmetry, and the parameters for the swimming behavior of soil bacterium Pseudomonas putida were based on literature values. Two different mechanisms for bacterial chemotaxis, one in which the bacteria responded to both positive and negative gradients, and the other in which they responded only to positive gradients, were compared. The results of the computer simulations showed that chemotaxis can increase migration through a porous medium in response to microscopic-scale gradients. The simulation results also suggested that a more significant role of chemotaxis may be to increase the residence time of the bacteria in the vicinity of an attractant source.     

Chemotaxis by Naegleria fowleri for Bacteria1

Naegleria fowleri amebae demonstrated a chemotactic and chemokinetic response toward live cells and extracts of Escherichia coli and other bacterial species when experiments were performed using a blind-well chemotaxis chamber. The peptide N-formyl-methionyl-leucyl-phenylalanine acted as a chemokinetic rather than a chemotactic factor for N. fowleri amebae. Competition experiments in which nerve cell extracts or bacteria were placed on either side of the filter in chemotaxis chambers resulted in increased movement towards bacteria. A scanning electron microscopy study of the interaction of N. fowleri with different bacterial species confirmed that when the amebae were near ingestible bacteria they moved toward the bacteria by pseudopod formation. Naegleria fowleri appeared to respond to bacteria by three interrelated but distinct processes: (a) chemokinesis, (b) chemotaxis, and (c) formation of food cups.     

Continuous-Flow Capillary Assay for Measuring Bacterial Chemotaxis

Bacterial chemotaxis may have a significant impact on the structure and function of bacterial communities. Quantification of chemotactic motion is necessary to identify chemoeffectors and to determine the bacterial transport parameters used in predictive models of chemotaxis. When the chemotactic bacteria consume the chemoeffector, the chemoeffector gradient to which the bacteria respond may be significantly perturbed by the consumption. Therefore, consumption of the chemoeffector can confound chemotaxis measurements if it is not accounted for. Current methods of quantifying chemotaxis use bacterial concentrations that are too high to preclude chemoeffector consumption or involve ill-defined conditions that make quantifying chemotaxis difficult. We developed a method of quantifying bacterial chemotaxis at low cell concentrations (~10⁵ CFU/ml), so metabolism of the chemoeffector is minimized. The method facilitates quantification of bacterial-transport parameters by providing well-defined boundary conditions and can be used with volatile and semivolatile chemoeffectors.     

Continuous-flow capillary assay for measuring bacterial chemotaxis

Bacterial chemotaxis may have a significant impact on the structure and function of bacterial communities. Quantification of chemotactic motion is necessary to identify chemoeffectors and to determine the bacterial transport parameters used in predictive models of chemotaxis. When the chemotactic bacteria consume the chemoeffector, the chemoeffector gradient to which the bacteria respond may be significantly perturbed by the consumption. Therefore, consumption of the chemoeffector can confound chemotaxis measurements if it is not accounted for. Current methods of quantifying chemotaxis use bacterial concentrations that are too high to preclude chemoeffector consumption or involve ill-defined conditions that make quantifying chemotaxis difficult. We developed a method of quantifying bacterial chemotaxis at low cell concentrations ( approximately 10(5) CFU/ml), so metabolism of the chemoeffector is minimized. The method facilitates quantification of bacterial-transport parameters by providing well-defined boundary conditions and can be used with volatile and semivolatile chemoeffectors.     

Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility

Myxococcus xanthus social (S) gliding motility has been previously reported by us to require the chemotaxis homologues encoded by the dif genes. In addition, two cell surface structures, type IV pili and extracellular matrix fibrils, are also critical to M. xanthus S motility. We have demonstrated here that M. xanthus dif genes are required for the biogenesis of fibrils but not for that of type IV pili. Furthermore, the developmental defects of dif mutants can be partially rescued by the addition of isolated fibril materials. Along with the chemotaxis genes of various swarming bacteria and the pilGHIJ genes of the twitching bacterium Pseudomonas aeruginosa, the M. xanthus dif genes belong to a unique class of bacterial chemotaxis genes or homologues implicated in the biogenesis of structures required for bacterial surface locomotion. Genetic studies indicate that the dif genes are linked to the M. xanthus dsp region, a locus known to be crucial for M. xanthus fibril biogenesis and S gliding.     

A hitchhiker's guide through advances and conceptual changes in chemotaxis

Chemotaxis is a basic recognition process, governed by protein network that translates molecular-based information on the surrounding environment into a guided motional response of the recipient cell or organism. This process is prevalent from bacteria to human beings. Some of the chemotaxis systems--like that of the bacterium Escherichia coli--are well established; others--like that of mammalian sperm cells--are at their relatively early stages of research. In contrast to mammalian sperm chemotaxis, where studies have so far been limited to the phenomenological level primarily, the model of bacterial chemotaxis is known down to the angstrom resolution. Despite this difference in depth of understanding, many fundamental questions are open not only in the new but also in the old chemotaxis fields of research, and recent advances in them are raising additional intriguing questions. This review summarizes some of these surprises and previously unasked or overlooked questions, and as such it offers a guided tour through conceptual changes in chemotaxis.     

Phototrophic consortia: model systems for symbiotic interrelations between prokaryotes

Most symbiotic prokaryotes known to date have been found in association with eukaryotes, whereas only few (3.5%) bacteria or archaea are known that have established interactions with other prokaryotes. As revealed by direct microscopic investigations, however, multiple morphotypes of highly structured associations of different prokaryotes exist in nature. These so-called consortia appear to represent the most developed type of bacterial interaction. Phototrophic consortia are associations of green sulfur bacteria that surround a central chemotrophic bacterium. In some natural environments, almost all cells of green sulfur bacteria occur in the associated state, i.e. as epibionts of phototrophic consortia. In contrast to earlier speculations, the central bacterium belongs to the beta-Proteobacteria. Within the consortia, the green sulfur bacterial epibionts grow photolithoautotrophically, utilizing exogenous sulfide as photosynthetic electron donor. The entire consortium does not appear to be independent of organic carbon compounds, since it exhibits chemotaxis towards 2-oxoglutarate and, as demonstrated by microautoradiography, can also incorporate this compound. Intact consortia exhibit a scotophobic response in which the bacteriochlorophylls of the epibionts function as light sensors, whereas the chemotrophic central bacterium confers motility upon the association. Hence, a signal exchange must occur between the different bacteria. Based on their 16S rRNA gene sequences, the epibionts represent distinct phylotypes that are often only distantly related to known species of green sulfur bacteria. Since phototrophic consortia have recently become available in enrichment cultures, they can now serve as suitable model systems for the investigation of the molecular mechanisms of cell-cell recognition and signal exchange, and for studies of the coevolution of nonrelated prokaryotes.     

A Multiple-Relaxation-Time Lattice-Boltzmann Model for Bacterial Chemotaxis: Effects of Initial Concentration,Diffusion, and Hydrodynamic Dispersion on Traveling Bacterial Bands

Bacterial chemotaxis can enhance the bioremediation of contaminants in aqueous and subsurface environments if the contaminant is a chemoattractant that the bacteria degrade. The process can be promoted by traveling bands of chemotactic bacteria that form due to metabolism-generated gradients in chemoattractant concentration. We developed a multiple-relaxation-time (MRT) lattice-Boltzmann method (LBM) to model chemotaxis, because LBMs are well suited to model reactive transport in the complex geometries that are typical for subsurface porous media. This MRT-LBM can attain a better numerical stability than its corresponding single-relaxation-time LBM. We performed simulations to investigate the effects of substrate diffusion, initial bacterial concentration, and hydrodynamic dispersion on the formation, shape, and propagation of bacterial bands. Band formation requires a sufficiently high initial number of bacteria and a small substrate diffusion coefficient. Uniform flow does not affect the bands while shear flow does. Bacterial bands can move both upstream and downstream when the flow velocity is small. However, the bands disappear once the velocity becomes too large due to hydrodynamic dispersion. Generally bands can only be observed if the dimensionless ratio between the chemotactic sensitivity coefficient and the effective diffusion coefficient of the bacteria exceeds a critical value, that is, when the biased movement due to chemotaxis overcomes the diffusion-like movement due to the random motility and hydrodynamic dispersion.     

Bacteria can form interconnected microcolonies when a self-excreted product reduces their surface motility: evidence from individual-based model simulations

Recent experimental observations of Pseudomonas aeruginosa, a model bacterium in biofilm research, reveal that, under specific growth conditions, bacterial cells form patterns of interconnected microcolonies. In the present work, we use an individual-based model to assess the involvement of bacteria motility and self-produced extracellular substance in the formation of these patterns. In our simulations, the pattern of interconnected microcolonies appears only when bacteria motility is reduced by excreted extracellular macromolecules. Immotile bacteria form isolated microcolonies and constantly motile bacteria form flat biofilms. Based on experimental data and computer simulations, we suggest a mechanism that could be responsible for these interconnected microcolonies.     

Ecology and Physics of Bacterial Chemotaxis in the Ocean

Summary: Intuitively, it may seem that from the perspective of an individual bacterium the ocean is a vast, dilute, and largely homogeneous environment. Microbial oceanographers have typically considered the ocean from this point of view. In reality, marine bacteria inhabit a chemical seascape that is highly heterogeneous down to the microscale, owing to ubiquitous nutrient patches, plumes, and gradients. Exudation and excretion of dissolved matter by larger organisms, lysis events, particles, animal surfaces, and fluxes from the sediment-water interface all contribute to create strong and pervasive heterogeneity, where chemotaxis may provide a significant fitness advantage to bacteria. The dynamic nature of the ocean imposes strong selective pressures on bacterial foraging strategies, and many marine bacteria indeed display adaptations that characterize their chemotactic motility as “high performance” compared to that of enteric model organisms. Fast swimming speeds, strongly directional responses, and effective turning and steering strategies ensure that marine bacteria can successfully use chemotaxis to very rapidly respond to chemical gradients in the ocean. These fast responses are advantageous in a broad range of ecological processes, including attaching to particles, exploiting particle plumes, retaining position close to phytoplankton cells, colonizing host animals, and hovering at a preferred height above the sediment-water interface. At larger scales, these responses can impact ocean biogeochemistry by increasing the rates of chemical transformation, influencing the flux of sinking material, and potentially altering the balance of biomass incorporation versus respiration. This review highlights the physical and ecological processes underpinning bacterial motility and chemotaxis in the ocean, describes the current state of knowledge of chemotaxis in marine bacteria, and summarizes our understanding of how these microscale dynamics scale up to affect ecosystem-scale processes in the sea.