Broadcasting of amplitude- and frequency-modulated c-di-GMP signals facilitates cooperative surface commitment in bacterial lineages
| Autor: | Calvin K. Lee, William C. Schmidt, Shanice S. Webster, Jonathan W. Chen, George A. O’Toole, Gerard C. L. Wong |
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| Rok vydání: | 2021 |
| Předmět: |
Multidisciplinary
bacteria biofilms cyclic-di-GMP Biological Sciences Bacterial Physiological Phenomena Microbiology Applied Physical Sciences Bacterial Proteins surface sensing motility Clinical Research Mutation Pseudomonas aeruginosa Physical Sciences 2.1 Biological and endogenous factors Aetiology Cyclic GMP Protein Binding Signal Transduction |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America Proceedings of the National Academy of Sciences of the United States of America, vol 119, iss 4 |
| ISSN: | 1091-6490 |
| Popis: | Significance It is well known that c-di-GMP concentration rises in surface-sensing bacteria and functions as a “molecular switch” for biofilm formation. Here, we provide an important recasting of this picture: Intracellular c-di-GMP signals do not just increase in surface-sensing bacteria; such signals are cooperatively broadcast across multiple generations of cells in a lineage with oscillations that undergo both amplitude and frequency modulation, which are controlled by the coupling between pili appendages and c-di-GMP synthesis machinery. The right “tuning” of these signals in terms of frequency and amplitude correlates ultimately to surface commitment. Amplitude and frequency modulation of c-di-GMP signals allows encoding of more complex instructions. Thus, our work provides a more nuanced understanding of how c-di-GMP signaling drives surface commitment. Work on surface sensing in bacterial biofilms has focused on how cells transduce sensory input into cyclic diguanylate (c-di-GMP) signaling, low and high levels of which generally correlate with high-motility planktonic cells and low-motility biofilm cells, respectively. Using Granger causal inference methods, however, we find that single-cell c-di-GMP increases are not sufficient to imply surface commitment. Tracking entire lineages of cells from the progenitor cell onward reveals that c-di-GMP levels can exhibit increases but also undergo oscillations that can propagate across 10 to 20 generations, thereby encoding more complex instructions for community behavior. Principal component and factor analysis of lineage c-di-GMP data shows that surface commitment behavior correlates with three statistically independent composite features, which roughly correspond to mean c-di-GMP levels, c-di-GMP oscillation period, and surface motility. Surface commitment in young biofilms does not correlate to c-di-GMP increases alone but also to the emergence of high-frequency and small-amplitude modulation of elevated c-di-GMP signal along a lineage of cells. Using this framework, we dissect how increasing or decreasing signal transduction from wild-type levels, by varying the interaction strength between PilO, a component of a principal surface sensing appendage system, and SadC, a key hub diguanylate cyclase that synthesizes c-di-GMP, impacts frequency and amplitude modulation of c-di-GMP signals and cooperative surface commitment. |
| Databáze: | OpenAIRE |
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