Integration of the Second Messenger c-di-GMP into the Chemotactic Signaling Pathway

Abstract

Elevated intracellular levels of the bacterial second messenger c-di-GMP are known to suppress motility and promote sessility. Bacterial chemotaxis guides motile cells in gradients of attractants and repellents over broad concentration ranges, thus allowing bacteria to quickly adapt to changes in their surroundings. Here, we describe a chemotaxis receptor that enhances, as opposed to suppresses, motility in response to temporary increases in intracellular c-di-GMP. Azospirillum brasilense’s preferred metabolism is adapted to microaerophily, and these motile cells quickly navigate to zones of low oxygen concentration by aerotaxis. We observed that changes in oxygen concentration result in rapid changes in intracellular c-di-GMP levels. The aerotaxis and chemotaxis receptor, Tlp1, binds c-di-GMP via its C-terminal PilZ domain and promotes persistent motility by increasing swimming velocity and decreasing swimming reversal frequency, which helps A. brasilense reach low-oxygen zones. If c-di-GMP levels remain high for extended periods, A. brasilense forms nonmotile clumps or biofilms on abiotic surfaces. These results suggest that association of increased c-di-GMP levels with sessility is correct on a long-term scale, while in the short-term c-di-GMP may actually promote, as opposed to suppress, motility. Our data suggest that sensing c-di-GMP by Tlp1 functions similar to methylation-based adaptation. Numerous chemotaxis receptors contain C-terminal PilZ domains or other sensory domains, suggesting that intracellular c-di-GMP as well as additional stimuli can be used to modulate adaptation of bacterial chemotaxis receptors.

Distinct Domains of CheA Confer Unique Functions in Chemotaxis and Cell Length in Azospirillum brasilense Sp7

“…Given its localization on the cell surface, the function of the membrane-anchored CheA1, while unknown, is expected to be independent of the chemotaxis signaling function of the protein, consistent with results obtained here. This hypothesis is further supported by the observation that chemotaxis receptor mutants that were shown to signal (e.g., Tlp1 [24] and AerC [25]) and localize at the cell poles (AerC [25]) in a Che1-dependent manner do not display any cell length phenotype, similar to those produced as a result of mutations in cheA1 (17).…”

“…Chemotactic rings were measured after 48 h of incubation. The temporal gradient assays for aerotaxis and computerized motion analysis were performed as previously described (24). Briefly, free-swimming cells were incubated on a slide placed inside a microchamber with an atmosphere of nitrogen gas (anaerobiosis) or air, which represents an attractant signal for the cells.…”

Chemotaxis Control of Transient Cell Aggregation

“…Consistent with this hypothesis, chemotaxis receptors modulating aggregation have been identified in Synechocystis (72), N. punctiforme (73), M. xanthus (74), and A. brasilense (75,76).…”

Internal Sense of Direction: Sensing and Signaling from Cytoplasmic Chemoreceptors

“…gand binding at C-terminal domains can influence chemoreceptor function (59). The diversity of domains in cytoplasmic chemoreceptors suggests that these proteins sense and integrate a wide group of intracellular signals.…”