Sticky situations: key components that control bacterial surface attachment

Abstract

The formation of bacterial biofilms is initiated by cells transitioning from the free-swimming mode of growth to a surface. This review is aimed at highlighting the common themes that have emerged in recent research regarding the key components, signals, and cues that aid in the transition and those involved in establishing a more permanent surface association during initial attachment.

Fig 1

Overview of events and factors playing a role in enabling bacteria to transition to the surface-associated lifestyle at a solid-liquid interface. To accomplish contact with the surface, bacteria first have to overcome the hydrodynamic boundary layer and repulsive forces as they approach the surface. Factors that accumulate in the conditioning film, compared to those of the bulk liquid, contribute to the decision of whether to commit to the surface or to leave. Reversible attachment is characterized by cells loosely attached via a single pole (resulting in a spinning motion) that may readily detach and return to the planktonic phase. Twitching motility is also observed. Surface contact is sensed via flagellar rotation being impeded due to close proximity and/or surface sensory proteins (e.g., NlpE). Transition to irreversible attachment is indicated by cells attached to the surface along their axis, with the resulting reduction in flagellar rotation triggering increased polysaccharide production and, potentially, c-di-GMP levels. This is followed by cells showing an aggregative behavior indicated by cell-to-cell contact and induction of quorum sensing. While the timing of events during this attachment stage has not been fully explored, it appears that the Lap and the SadBC/BifA systems are essential for the transition to the irreversible attachment stage.

Fig 2

Model for inorganic-phosphate (P_i)- and Lap-mediated control of biofilm formation in soil pseudomonads. In high P_i conditions (right), c-di-GMP accumulates in the cell, probably via the DGCs GcbB and GcbC. LapD binds c-di-GMP via its EAL domain and sequesters LapG at the inner membrane, promoting the maintenance of the LapA adhesin on the cell surface and, thus, fostering biofilm formation. When low extracellular P_i is sensed (left) by the Pho system, activated PhoR promotes rapA transcription via PhoB. The PDE activity of RapA depletes cellular c-di-GMP and leads to the dissociation of c-di-GMP from LapD and a conformational change of LapD. In the absence of bound c-di-GMP, LapD is unable to interact with the protease LapG, and LapG, in turn, cleaves the N terminus of LapA in the periplasm, promoting its loss from the cell surface. Release of LapA from attached cells promotes their detachment from the substratum and bacteria returning to the free-swimming mode of growth. The model is based on structural and functional analyses (50, 62, 109, 116, 118).