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Particulate organic carbon settling through the marine water column is a key process that regulates the global climate by sequestering atmospheric carbon. The initial colonization of marine particles by heterotrophic bacteria represents the first step in recycling this carbon back to inorganic constituents—setting the magnitude of vertical carbon transport to the abyss. Here, we demonstrate experimentally using millifluidic devices that, although bacterial motility is essential for effective colonization of a particle leaking organic nutrients into the water column, chemotaxis specifically benefits at intermediate and higher settling velocities to navigate the particle boundary layer during the brief window of opportunity provided by a passing particle. We develop an individual-based model that simulates the encounter and attachment of bacterial cells with leaking marine particles to systematically evaluate the role of different parameters associated with bacterial run-and-tumble motility. We further use this model to explore the role of particle microstructure on the colonization efficiency of bacteria with different motility traits. We find that the porous microstructure facilitates additional colonization by chemotactic and motile bacteria, and fundamentally alters the way nonmotile cells interact with particles due to streamlines intersecting with the particle surface.

 

ABSTRACT In aquatic environments, Caulobacter spp. can be found at the boundary between liquid and air known as the neuston. I report an approach to study temporal features of Caulobacter crescentus colonization and pellicle biofilm development at the air-liquid interface and have defined the role of cell surface structures in this process. At this interface, C. crescentus initially forms a monolayer of cells bearing a surface adhesin known as the holdfast. When excised from the liquid surface, this monolayer strongly adheres to glass. The monolayer subsequently develops into a three-dimensional structure that is highly enriched in clusters of stalked cells known as rosettes. As this pellicle film matures, it becomes more cohesive and less adherent to a glass surface. A mutant strain lacking a flagellum does not efficiently reach the surface, and strains lacking type IV pili exhibit defects in organization of the three-dimensional pellicle. Strains unable to synthesize the holdfast fail to accumulate at the boundary between air and liquid and do not form a pellicle. Phase-contrast images support a model whereby the holdfast functions to trap C. crescentus cells at the air-liquid boundary. Unlike the holdfast, neither the flagellum nor type IV pili are required for C. crescentus to partition to the air-liquid interface. While it is well established that the holdfast enables adherence to solid surfaces, this study provides evidence that the holdfast has physicochemical properties that allow partitioning of nonmotile mother cells to the air-liquid interface and facilitate colonization of this microenvironment. IMPORTANCE In aquatic environments, the boundary at the air interface is often highly enriched with nutrients and oxygen. Colonization of this niche likely confers a significant fitness advantage in many cases. This study provides evidence that the cell surface adhesin known as a holdfast enables Caulobacter crescentus to partition to and colonize the air-liquid interface. Additional surface structures, including the flagellum and type IV pili, are important determinants of colonization and biofilm formation at this boundary. Considering that holdfast-like adhesins are broadly conserved in Caulobacter spp. and other members of the diverse class Alphaproteobacteria , these surface structures may function broadly to facilitate colonization of air-liquid boundaries in a range of ecological contexts, including freshwater, marine, and soil ecosystems. 

ABSTRACT Bacteria form complex multicellular structures on solid surfaces known as biofilms, which allow them to survive in harsh environments. A hallmark characteristic of mature biofilms is the high-level antibiotic tolerance (up to 1,000 times) compared with that of planktonic cells. Here, we report our new findings that biofilm cells are not always more tolerant to antibiotics than planktonic cells in the same culture. Specifically, Escherichia coli RP437 exhibited a dynamic change in antibiotic susceptibility during its early-stage biofilm formation. This phenomenon was not strain specific. Upon initial attachment, surface-associated cells became more sensitive to antibiotics than planktonic cells. By controlling the cell adhesion and cluster size using patterned E. coli biofilms, cells involved in the interaction between cell clusters during microcolony formation were found to be more susceptible to ampicillin than cells within clusters, suggesting a role of cell-cell interactions in biofilm-associated antibiotic tolerance. After this stage, biofilm cells became less susceptible to ampicillin and ofloxacin than planktonic cells. However, when the cells were detached by sonication, both antibiotics were more effective in killing the detached biofilm cells than the planktonic cells. Collectively, these results indicate that biofilm formation involves active cellular activities in adaption to the attached life form and interactions between cell clusters to build the complex structure of a biofilm, which can render these cells more susceptible to antibiotics. These findings shed new light on bacterial antibiotic susceptibility during biofilm formation and can guide the design of better antifouling surfaces, e.g., those with micron-scale topographic structures to interrupt cell-cell interactions. IMPORTANCE Mature biofilms are known for their high-level tolerance to antibiotics; however, antibiotic susceptibility of sessile cells during early-stage biofilm formation is not well understood. In this study, we aim to fill this knowledge gap by following bacterial antibiotic susceptibility during early-stage biofilm formation. We found that the attached cells have a dynamic change in antibiotic susceptibility, and during certain phases, they can be more sensitive to antibiotics than planktonic counterparts in the same culture. Using surface chemistry-controlled patterned biofilm formation, cell-surface and cell-cell interactions were found to affect the antibiotic susceptibility of attached cells. Collectively, these findings provide new insights into biofilm physiology and reveal how adaptation to the attached life form may influence antibiotic susceptibility of bacterial cells. 

ABSTRACT The 6th American Society for Microbiology Conference on Cell-Cell Communication in Bacteria convened from 16 to 19 October 2017 in Athens, GA. In this minireview, we highlight some of the research presented at that meeting that addresses central questions emerging in the field, including the following questions. How are cell-cell communication circuits designed to generate responses? Where are bacteria communicating? Finally, why are bacteria engaging in such behaviors? 

Bacterial biofilms are communities of bacteria that exist as aggregates that can adhere to surfaces or be free-standing. This complex, social mode of cellular organization is fundamental to the physiology of microbes and often exhibits surprising behaviour. Bacterial biofilms are more than the sum of their parts: Single cell behaviour has a complex relation to collective community behaviour, in a manner perhaps cognate to the complex relation between atomic physics and condensed matter physics. Biofilm microbiology is a relatively young field by biology standards, but it has already attracted intense attention from physicists. Sometimes, this attention takes the form of seeing biofilms as inspiration for new physics. In this roadmap, we highlight the work of those who have taken the opposite strategy: We highlight work of physicists and physical scientists who use physics to engage fundamental concepts in bacterial biofilm microbiology, including adhesion, sensing, motility, signalling, memory, energy flow, community formation and cooperativity. These contributions are juxtaposed with microbiologists who have made recent important discoveries on bacterial biofilms using state-of-the-art physical methods. The contributions to this roadmap exemplify how well physics and biology can be combined to achieve a new synthesis, rather than just a division of labour.