Role of Caulobacter Cell Surface Structures in Colonization of the Air-Liquid Interface

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.

Regulation of bacterial surface attachment by a network of sensory transduction proteins

“…Holdfast-mediated adherence to solid surfaces is permanent [9–11]. The holdfast enables cell attachment to a variety of chemically diverse materials [12], and also facilitates partitioning of cells to the air-liquid interface in aqueous media [13]. C .…”

Regulation of bacterial surface attachment by a network of sensory transduction proteins

“…Swarmer cells differentiate into stalked cells, whereupon they can secrete a unipolar polysaccharide adhesin known as the holdfast [5][6][7][8] (Fig 1A). Holdfast mediated adherence to solid surfaces is permanent [9][10][11]; the holdfast enables cell attachment to a variety of chemically diverse materials [12], and facilitates partitioning of cells to the air-liquid interface in aqueous medium [13]. C. crescentus tightly regulates holdfast synthesis and thus the transition between a planktonic and a surface-attached lifestyle, which likely reduces the probability of becoming restricted to a sub-optimal environment.…”

Production and molecular composition of Burkholderia pseudomallei and Burkholderia thailandensis biofilms

“…This suggests that temperature amongst other environmental conditions indicative of the two different environments may play a role in determining the type of biofilm formed. In Salmonella , curli is responsible for the switch [68] whereas, in C. crescentus, biofilm is initially formed as a monolayer of cells that subsequently develop into a three-dimensional structure and as the biofilm matures, it becomes more cohesive and less adherent [69]. Previous studies have confirmed that some pellicles of some organisms are composed of eDNA with close cell contact [23], sucrose, and proteins [70].…”