Reduced Water Availability Influences the Dynamics, Development, and Ultrastructural Properties of Pseudomonas putida Biofilms

Abstract

Pseudomonas putida strain mt-2 unsaturated biofilm formation proceeds through three distinct developmental phases, culminating in the formation of a microcolony. The form and severity of reduced water availability alter cell morphology, which influences microcolony size and ultrastructure. The dehydration (matric stress) treatments resulted in biofilms comprised of smaller cells, but they were taller and more porous and had a thicker extracellular polysaccharide layer at the air interface. In the solute stress treatments, cell filamentation occurred more frequently in the presence of high concentrations of ionic (but not nonionic) solutes, and these filamented cells drastically altered the biofilm architecture.In terrestrial habitats, bacteria reside on soil matrices or plant surfaces as aggregates of cells, or microcolonies, that are frequently enmeshed in exopolymeric substances of their own making and can be described as biofilms (1,5,19,23). These biofilms are commonly unsaturated, although water films, which vary in thickness depending on the environmental conditions, surround them. In a saturated system, the water potential is comprised almost exclusively of the solute potential (24). However, under unsaturated conditions, water availability is influenced by both the solute and matric potentials (24). The difference between these two stresses is that with a solute stress, bacteria are bathed in water of diminished activity but that with a matric stress, bacteria are dehydrated due to low water contents and the availability of the water is reduced through its interaction with the matrix. Under normal conditions, soil bacteria experience significant matric stress (12).In aquatic systems, channels in the biofilm act as conduits for waste removal and nutrient supply (34). Under low-shear laminar flow, Pseudomonas aeruginosa PAO1 biofilms consist of a monolayer of cells with mound-shaped, circular microcolonies, but under high-shear turbulent flow, PAO1 biofilms consist of filamentous streamers (8,14,25). The development of this complex architecture is influenced by hydrodynamics, nutrient composition, and biological properties such as quorum sensing, extracellular polysaccharide (EPS) production, and motility (8). In unsaturated habitats, the lack of laminar fluid flow dramatically influences nutrient availability patterns, metabolic-waste accumulation and disposal, and the accumulation of cell-signaling molecules and, consequently, biofilm architecture.Atomic-force microscopy of fresh and desiccated Pseudomonas putida biofilms revealed that drying had little effect on physical morphology and surface properties (1). However, those studies focused on fully developed, mature biofilms that were then dried. In many ways, the growth of bacteria on agar surfaces better approximates the conditions that bacteria experience in many unsaturated habitats; they are able to acquire nutrients from the underlying matrix and from a relatively thin water film covering the biofilm. Examination of the organization of cells withi...

Hydration dynamics promote bacterial coexistence on rough surfaces

“…Hydration status and pore-space characteristics are critical factors shaping nutrient fields and bacterial motility, and are thus key to understanding bacterial interactions in soil and other porous media such as dry food products (Barton and Ford, 1997;Dens and Van Impe, 2000;Wilson et al, 2002;Chang and Halverson, 2003;Or et al, 2007;Chen and Jin, 2011). Although motility has long been argued as a key factor for survival in heterogeneous environments and for biodiversity maintenance (Fenchel, 2002;Reichenbach et al, 2007;Vos and Velicer, 2008), it is only recently that crucial processes regulating bacterial motility within liquid films forming on partially hydrated rough surfaces have been quantified (Dechesne et al, 2010;Wang and Or, 2010).…”

Formation of specialized aerial architectures by Rhodococcus during utilization of vaporized p-cresol

“…This orientation probably provides more surface area for cells to efficiently take up the p-cresol vapour and minerals from the agar surface. A similar arrangement of cells has been observed in the early stages of microcolony development by Escherichia coli and Pseudomonas putida (Chang & Halverson, 2003;Shapiro & Hsu, 1989). When the SAA were in actively growing stages, most long cells, including Y-shaped cells, were twisted in upright positions.…”

“…2C2). Perpendicular cell arrangements have been observed in other multicellular structures, including colonies and biofilms (Chang & Halverson, 2003;Enos-Berlage & McCarter, 2000;Lee & Veeranagouda, 2009). Closer examination of the images of the stalk of the SAA revealed that the short rod cells that were less than 1 mm in diameter had a more regularly compact arrangement (Fig.…”

Biocontrol of Fusarium wilt of banana: Key influence factors and strategies

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