Multigenerational memory and adaptive adhesion in early bacterial biofilm communities

Abstract

Using multigenerational, single-cell tracking we explore the earliest events of biofilm formation by During initial stages of surface engagement (≤20 h), the surface cell population of this microbe comprises overwhelmingly cells that attach poorly (∼95% stay<30 s, well below the ∼1-h division time) with little increase in surface population. If we harvest cells previously exposed to a surface and direct them to a virgin surface, we find that these surface-exposed cells and their descendants attach strongly and then rapidly increase the surface cell population. This "adaptive," time-delayed adhesion requires determinants we showed previously are critical for surface sensing: type IV pili (TFP) and cAMP signaling via the Pil-Chp-TFP system. We show that these surface-adapted cells exhibit damped, coupled out-of-phase oscillations of intracellular cAMP levels and associated TFP activity that persist for multiple generations, whereas surface-naïve cells show uncorrelated cAMP and TFP activity. These correlated cAMP-TFP oscillations, which effectively impart intergenerational memory to cells in a lineage, can be understood in terms of a Turing stochastic model based on the Pil-Chp-TFP framework. Importantly, these cAMP-TFP oscillations create a state characterized by a suppression of TFP motility coordinated across entire lineages and lead to a drastic increase in the number of surface-associated cells with near-zero translational motion. The appearance of this surface-adapted state, which can serve to define the historical classification of "irreversibly attached" cells, correlates with family tree architectures that facilitate exponential increases in surface cell populations necessary for biofilm formation.

cGAMP signaling controls a transient surface-associated lifestyle

“…These phenotypes contrast with the involvement of a canonical cdiG-synthesizing GGDEF enzyme, EsnD, in biofilm-based electricity production on electrodes (Chan et al, 2017). Along with growing evidence that transient-attached and permanent-attached states are distinct stages in the biofilm lifestyles of bacteria (Lee et al, 2018), this study provides the first evidence that these modes can be signaled by two different cyclic dinucleotides. Whether this paradigm is more widespread or whether other mechanisms are present in other bacteria is the subject of future work.…”

Modulation of Flagellar Rotation in Surface-Attached Bacteria: A Circuit for Rapid Surface-Sensing

“…cAMP signals in surface-associated bacteria are amplified by the Pil/Chp system, which mechano-senses via the retraction of T4P [48,49], and lead to surface-associated motility and virulence. Transient "surface-exposure" by swimming cells, however, also changes cAMP levels in individual bacteria that fail to commit to a surface, as recently demonstrated by Lee et al [50]. These so-called "surface-sentient" cells exhibit higher levels of intracellular cAMP and are more likely to progress to surface association and irreversible attachment on subsequent encounters with a surface.…”

Bacterial secretins: Mechanisms of assembly and membrane targeting

“…Type IV pili (T4P) are highly dynamic, and possess the remarkable ability to quickly extend and retract repeatedly. This ability is crucial for multiple functions, including adherence, motility, DNA uptake, and protein secretion …”