Dataset Information

Control of bacterial exoelectrogenesis by c-AMP-GMP.

ABSTRACT: Major changes in bacterial physiology including biofilm and spore formation involve signaling by the cyclic dinucleotides c-di-GMP and c-di-AMP. Recently, another second messenger dinucleotide, c-AMP-GMP, was found to control chemotaxis and colonization by Vibrio cholerae. We have identified a superregulon of genes controlled by c-AMP-GMP in numerous Deltaproteobacteria, including Geobacter species that use extracellular insoluble metal oxides as terminal electron acceptors. This exoelectrogenic process has been studied for its possible utility in energy production and bioremediation. Many genes involved in adhesion, pilin formation, and others that are important for exoelectrogenesis are controlled by members of a variant riboswitch class that selectively bind c-AMP-GMP. These RNAs constitute, to our knowledge, the first known specific receptors for c-AMP-GMP and reveal that this molecule is used by many bacteria to control specialized physiological processes.

SUBMITTER: Nelson JW

PROVIDER: S-EPMC4418907 | biostudies-literature | 2015 Apr

REPOSITORIES: biostudies-literature

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Control of bacterial exoelectrogenesis by c-AMP-GMP.

Nelson James W JW Sudarsan Narasimhan N Phillips Grace E GE Stav Shira S Lünse Christina E CE McCown Phillip J PJ Breaker Ronald R RR

Proceedings of the National Academy of Sciences of the United States of America 20150406 17

Major changes in bacterial physiology including biofilm and spore formation involve signaling by the cyclic dinucleotides c-di-GMP and c-di-AMP. Recently, another second messenger dinucleotide, c-AMP-GMP, was found to control chemotaxis and colonization by Vibrio cholerae. We have identified a superregulon of genes controlled by c-AMP-GMP in numerous Deltaproteobacteria, including Geobacter species that use extracellular insoluble metal oxides as terminal electron acceptors. This exoelectrogenic ...[more]

PMID: 25848023

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Project description:Bacterial motility has great medical and ecological significance because of its essential role in bacterial survival and pathogenesis. Cyclic dimeric GMP (c-di-GMP), a second messenger in bacteria, is the predominant regulator of flagellar synthesis and motility and possesses turnover mechanisms that have been thoroughly investigated. Therefore, much attention has been focused on identifying the upstream stimulatory signals and downstream modules that respond to altered c-di-GMP levels. Here, we systematically analyzed c-di-GMP cyclases and phosphodiesterases in Stenotrophomonas maltophilia to screen for motility regulators. Of these enzymes, we identified and characterized a new phosphodiesterase named SisP, which was found to facilitate bacterial swimming upon stimulation with ferrous iron. SisP-mediated degradation of c-di-GMP leads to FsnR-dependent transcription of flagellar genes. Remarkably, c-di-GMP controls FsnR via two independent mechanisms: by direct binding and indirectly by modulating its phosphorylation state. In this study, we deciphered a novel "one stone, two birds" regulatory strategy of c-di-GMP and uncovered the signal that stimulates c-di-GMP hydrolysis. Facilitation of bacterial swimming motility by ferrous iron might contribute to the higher risk of bacterial infection in acutely ill patients. IMPORTANCE Stenotrophomonas maltophilia has become a great threat to human health because of the high mortality of infected patients. Swimming motility plays a crucial role in regulating bacterial virulence and adaptation. However, limited progress has been made in cyclic dimeric GMP (c-di-GMP) controlling swimming motility of S. maltophilia. Here, we characterized c-di-GMP turnover enzymes encoded by S. maltophilia and dissected the regulatory details of a phosphodiesterase named SisP. We demonstrated that SisP degrades c-di-GMP to fully activate FsnR through directly releasing FsnR from the FsnR-c-di-GMP complex and indirectly increasing its phosphorylation level. This finding uncovered a quantitative, rather than an on-off, regulatory manner employed by c-di-GMP to regulate activities of its effectors. Identification of the specific activation of SisP by ferrous iron proposes SisP as a putative drug-target for controlling bacterial infection and ferrous iron at the wounds or cuts as a putative factor contributing to the higher risk of bacterial infection.

Dataset Information

Control of bacterial exoelectrogenesis by c-AMP-GMP.

Publications

Control of bacterial exoelectrogenesis by c-AMP-GMP.

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