Discovery of a Nitric Oxide Responsive Quorum Sensing Circuit in <i>Vibrio cholerae</i>

Henares, Bernadette M.; Higgins, Kate E.; Boon, Elizabeth M.

doi:10.1021/acschembio.8b00360

Cited by 49 publications

(43 citation statements)

References 29 publications

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“…The study of H‐NOX‐dependent signaling also continues to expand in various directions, including the discovery of another H‐NOX‐like NO sensing protein, NosP (NO signaling protein), by Hossain and Boon . NosPs are FIST domain‐containing proteins found in various bacteria, including several that harbor an H‐NOX .…”

Section: Discussionmentioning

confidence: 99%

“…It also inhibits the phosphotransfer from downstream histidine kinase NaHK to phosphotransfer protein HptB and regulates NO‐dependent biofilm formation . NosP from Vibrio cholerae has also been recently demonstrated to contribute to quorum sensing through interaction with a soluble kinase, VpsS . H‐NOX and NosP are both gas‐sensing proteins that are directly involved in biofilm formation.…”

Section: Discussionmentioning

confidence: 99%

“…The study of H-NOX-dependent signaling also continues to expand in various directions, including the discoveryo fa nother H-NOX-like NO sensing protein, NosP (NO signaling protein), by Hossain and Boon. [94,95] NosPs are FIST domain-containing proteins found in variousb acteria, including severalt hat harbor an H-NOX. [96] Bioinformatics analysisshowed that similar to H-NOXs, NosP domains/proteins are often associated with signaling proteins such as histidine kinases,d iguanylate cyclases and MCPs, suggesting that it could have the ability to regulate the activity of those proteins in trans.…”

Section: Discussionmentioning

confidence: 99%

“…[94] NosP from Vibrio cholerae has also been recently demonstrated to contributet oq uorum sensing through interaction with as oluble kinase, VpsS. [95] H-NOX and NosP are both gassensing proteins that are directly involved in biofilm formation. Further investigation is certainly needed to reveal their roles in NO signaling, the interaction with signaling partnersa nd the communication between the two pathways.…”

Section: Discussionmentioning

confidence: 99%

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Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation

Guo

Marletta

2018

ChemBioChem

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Heme‐nitric oxide/oxygen binding (H‐NOX) proteins are a family of gas‐binding hemoproteins that bind diatomic gas ligands such as nitric oxide (NO) and oxygen (O2). In bacteria, H‐NOXs are often associated with signaling partners, including histidine kinases (HKs), diguanylate cyclases (DGCs) or methyl‐accepting chemotaxis proteins (MCPs), either as a stand‐alone protein or as a domain of a larger polypeptide. H‐NOXs regulate the activity of cognate signaling proteins through ligand‐induced conformational changes in the H‐NOX domain and protein/protein interactions between the H‐NOX and the cognate signaling partner. This review summarizes recent progress toward deciphering the molecular mechanism of bacterial H‐NOX activation and the subsequent regulation of H‐NOX‐associated cognate sensor proteins from a structural and biochemical point of view.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation

Guo

Marletta

2018

ChemBioChem

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“…86 In our laboratory, we have found that, when ligated to NO, NosP from V. cholerae inhibits the autophosphorylation activity of this quorum sensing histidine kinase, suggesting a potential molecular mechanism by which NO may regulate quorum sensing (and thus biofilm formation) in V. cholera . 92 Interestingly, this would be analogous to the NO and H-NOX/HqsK mediated quorum sensing pathway we discovered in V. harveyi . 54 …”

Section: Nitric Oxide and Nosp Signaling In Bacterial Biofilmsmentioning

confidence: 74%

Discovery of Two Bacterial Nitric Oxide-Responsive Proteins and Their Roles in Bacterial Biofilm Regulation

2017

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CONSPECTUS Bacterial biofilms form when bacteria adhere to a surface and produce an exopolysaccharide matrix (Costerton et al. Science 1999, 284, 1318; Davies et al. Science 1998, 280, 295; Flemming et al. Nat. Rev. Microbiol. 2010, 8, 623). Because biofilms are resistant to antibiotics, they are problematic in many aspects of human health and welfare, causing, for instance, persistent fouling of medical implants such as catheters and artificial joints (Brunetto et al. Chimia 2008, 62, 249). They are responsible for chronic infections in the lungs of cystic fibrosis patients and in open wounds, such as those associated with burns and diabetes. They are also a major contributor to hospital-acquired infections (Sievert et al. Infec. Control Hosp. Epidemiol. 2013, 34, 1; Tatterson et al. Front. Biosci. 2001, 6, D890). It has been hypothesized that effective methods of biofilm control will have widespread application (Landini et al. Appl. Microbiol. Biotechnol. 2010, 86, 813). A promising strategy is to target the mechanisms that drive biofilm dispersal, because dispersal results in biofilm removal and in the restoration of antibiotic sensitivity. First documented in Nitrosomonas europaea (Schmidt et al. J. Bacteriol. 2004, 186, 2781) and the cystic fibrosis-associated pathogen Pseudomonas aeruginosa (Barraud et al. J. Bacteriol. 2006, 188, 7344; J. Bacteriol. 2009, 191, 7333), regulation of biofilm formation by nanomolar levels of the diatomic gas nitric oxide (NO) has now been documented in numerous bacteria (Barraud et al. Microb. Biotechnol. 2009, 2, 370; McDougald et al. Nat. Rev. Microbiol. 2012, 10, 39; Arora et al. Biochemistry 2015, 54, 3717; Barraud et al. Curr. Pharm. Des. 2015, 21, 31). NO-mediated pathways are, therefore, promising candidates for biofilm regulation. Characterization of the NO sensors and NO-regulated signaling pathways should allow for rational manipulation of these pathways for therapeutic applications. Several laboratories, including our own, have shown that a class of NO sensors called H-NOX (heme-nitric oxide or oxygen binding domain) affects biofilm formation by regulating intracellular cyclic di-GMP concentrations and quorum sensing (Arora et al. Biochemistry 2015, 54, 3717; Plate et al. Trends Biochem. Sci. 2013, 38, 566; Nisbett et al. Biochemistry 2016, 55, 4873). Many bacteria that respond to NO do not encode an hnoX gene, however. My laboratory has now discovered an additional family of bacterial NO sensors, called NosP (nitric oxide sensing protein). Importantly, NosP domains are widely conserved in bacteria, especially Gram-negative bacteria, where they are encoded as fusions with or in close chromosomal proximity to histidine kinases or cyclic di-GMP synthesis or phosphodiesterase enzyme, consistent with signaling. In this Account, we briefly review NO and HNOX signaling in bacterial biofilms, describe our discovery of the NosP family, and provide support for its role in biofilm regulation in Pseudomonas aeruginosa, Vibrio cholerae, Legionella pneumophila, and Shewanella o...

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Physiological Roles of Nitrite and Nitric Oxide in Bacteria: Similar Consequences from Distinct Cell Targets, Protection, and Sensing Systems

Guo

Gao

2021

Advanced Biology

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sodium nitrite) is currently in a phase 2b clinical trial as a drug for pulmonary hypertension treatment on the basis of the finding that it could be safely applied to reach millimolar concentrations in the airway surface liquid. [6] In the broad nitrogen biogeochemical cycle, nitrite serves as the central molecule linking nitrate (NO 3 − ) to dinitrogen gas (N 2 ) or ammonia (NH 3 ). [7] As a nitrogen oxo-anion, nitrite per se is crucial to life on earth because it participates in diverse key biological processes, especially in bacteria because they are renowned for their ability to carry out biological transformation of nitrite (Maia and Moura, 2014). Nitrite can be oxidized to nitrate or reduced to various nitrogen species such as nitric oxide (NO), nitrous oxide (N 2 O), N 2 , and NH 3 . [8] Although nitrite transformation is regarded as an effective means for detoxification, it brings out new threats. [7] Apart from an intermediate in the nitrogen cycle, NO, whose physiological concentrations are suggested to be up to ≈5 nM in cells, is a well-recognized bacteriostatic agent the same as nitrite. [9] It should be noted that concentrations of NO generated from nitrite reduction vary drastically in different bacteria, for example, less than 20 nM and up to 38 µM in cultures of two denitrifiers Paracoccus denitrificans and Agrobacterium tumefaciens, respectively. [10] In bacteria, a variety of enzymes are implicated in generation of NO from nitrite, and consistently, multiple enzymes contribute to transformation of NO to other nitrogen species for detoxification. [7,11] It is worth noting that in contrast to nitrite, whose transformation is exclusively conducted by enzymes involved in the nitrogen biogeochemical cycle, NO can be generated and scavenged by proteins outside the cycle, bacterial NO synthases (bNOSs) and flavohemoglobin Hmp, respectively. [12] Both nitrite and NO are bacteriostatic agents due to their ability to inhibit protein activity. In vitro studies show that nitrite and NO display similar, albeit not identical, biochemical properties, and therefore proteins susceptible to them are similar, mainly those containing redox-active centers such as heme, iron-sulfur clusters, mono-/di-nuclear iron, thiol, and so on. [13] Consistently, most of cellular targets identified in vivo are metabolic and respiratory enzymes depending on their redox-active centers for catalysis and/or oxi-reduction. [11] Despite this, cellular targets of nitrite and NO in any given bacterial species are Nitrite and nitric oxide (NO) are two active nitrogen oxides that display similar biochemical properties, especially when interacting with redox-sensitive proteins (i.e., hemoproteins), an observation serving as the foundation of the notion that the antibacterial effect of nitrite is largely attributed to NO formation. However, a growing body of evidence suggests that they are largely treated as distinct molecules by bacterial cells. Although both nitrite and NO are formed and decomposed by enzymes participating in the trans...

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Discovery of a Nitric Oxide Responsive Quorum Sensing Circuit in Vibrio cholerae

Cited by 49 publications

References 29 publications

Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation

Structural Insight into H‐NOX Gas Sensing and Cognate Signaling Protein Regulation

Discovery of Two Bacterial Nitric Oxide-Responsive Proteins and Their Roles in Bacterial Biofilm Regulation

Physiological Roles of Nitrite and Nitric Oxide in Bacteria: Similar Consequences from Distinct Cell Targets, Protection, and Sensing Systems

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