Two-Dimensional Patterns in Bacterial Veils Arise from Self-generated, Three-Dimensional Fluid Flows

Abstract

The behavior of collections of oceanic bacteria is controlled by metabolic (chemotaxis) and physical (fluid motion) processes. Some sulfur-oxidizing bacteria, such as Thiovulum majus, unite these two processes via a material interface produced by the bacteria and upon which the bacteria are transiently attached. This interface, termed a bacterial veil, is formed by exo-polymeric substances (EPS) produced by the bacteria. By adhering to the veil while continuing to rotate their flagella, the bacteria are able to exert force on the fluid surroundings. This behavior induces a fluid flow that, in turn, causes the bacteria to aggregate leading to the formation of a physical pattern in the veil. These striking patterns are very similar in flavor to the classic convection instability observed when a shallow fluid is heated from below. However, the physics are very different since the flow around the veil is mediated by the bacteria and affects the bacterial densities. In this study, we extend a model of a one-dimensional veil in a two-dimensional fluid to the more realistic two-dimensional veil in a three-dimensional fluid. The linear stability analysis indicates that the Peclet number serves as a bifurcation parameter, which is consistent with experimental observations. We also solve the nonlinear problem numerically and are able to obtain patterns that are similar to those observed in the experiments.

Hydrodynamics and collective behavior of the tethered bacteriumThiovulum majus

“…This model differs substantially from a previous model of T. majus dynamics proposed by Cogan and Wolgemuth (24,26). In their model, interactions between cells are mediated by the flow of water.…”

“…An individual cell exerting a force of f 0 ≈ 40 pN experiences a Péclet number of Pe ∼ 1. However, when cells tether to a veil, variations in cell density drive large-scale flows that stir the environment (17,26). Remarkably, natural veils are observed to generate millimeter-scale flows that pull oxygen through the water with Péclet number Pe ∼ 40 (17).…”

“…Cells in a T. majus community generate millimeter-scale convective flows that pull nutrient-rich water to cells (17). Despite interest in the ecology (19,20), motility (21)(22)(23), physiology (14,15), and community morphology (24)(25)(26) of these bacteria, relatively little is understood about how the dynamics of T. majus cells give rise to collective phenomena. Past studies have been hampered by the difficulty in enriching T. majus from environmental samples.…”

Nucleation of rotating crystals byThiovulum majusbacteria

“…Thiovulum majus [1][2][3] is one of the fastest-swimming bacteria in the world, reaching speeds of up to m 600 m s −1 [4,5]. As such, the physical basis of its motion, both individually [6][7][8][9][10][11] and collectively [12][13][14][15][16][17][18], is of interest from both biological and physical perspectives. When these bacteria are confined between a glass slide and cover slip, cells localize on the glass surfaces and self organize into active crystals composed of rotating cells ( figure 1(a)), which spin and reorganize [19].…”

Excitation and Adaptation in Bacteria–a Model Signal Transduction System that Controls Taxis and Spatial Pattern Formation

“…In this section, we review biological experiments and mathematical models for the patterns formed by cells such as E. coli that use a run-and-tumble strategy. Pattern formation in other bacterial colonies, e.g., Bacillus , Proteus and Myxococcus , and mathematical models of more complicated biofilms are discussed in [155–165]. …”