NosP Signaling Modulates the NO/H-NOX-Mediated Multicomponent c-Di-GMP Network and Biofilm Formation in <i>Shewanella oneidensis</i>

Nisbett, Lisa-Marie; Binnenkade, Lucas; Bacon, Bezalel; Hossain, S. M. Zakir; Kotloski, Nicholas J.; Brutinel, Evan D.; Hartmann, Raimo; Drescher, Knut; Arora, Dhruv P.; Muralidharan, Sandhya; Thormann, Kai M.; Gralnick, Jeffrey A.; Boon, Elizabeth M.

doi:10.1021/acs.biochem.9b00706

Cited by 21 publications

(28 citation statements)

References 49 publications

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“…A subfamily of H-NOX sensors found in facultative anaerobes (such as Shewanella oneidensis and Vibrio cholerae ) are specific NO sensors that do not form a stable complex with O 2 similarly with sGC. The function of such bacterial H-NOX proteins is thought to regulate biofilm formation or quorum sensing signaling in a NO-dependent manner 9 , 10 . Another subfamily of H-NOX sensors was found in obligate anaerobes such as Caldanaerobacter subterraneus subsp.…”

Section: Introductionmentioning

confidence: 99%

Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium

et al. 2021

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Heme-Nitric oxide and Oxygen binding protein domains (H-NOX) are found in signaling pathways of both prokaryotes and eukaryotes and share sequence homology with soluble guanylate cyclase, the mammalian NO receptor. In bacteria, H-NOX is associated with kinase or methyl accepting chemotaxis domains. In the O2-sensor of the strict anaerobe Caldanaerobacter tengcongensis (Ct H-NOX) the heme appears highly distorted after O2 binding, but the role of heme distortion in allosteric transitions was not yet evidenced. Here, we measure the dynamics of the heme distortion triggered by the dissociation of diatomics from Ct H-NOX using transient electronic absorption spectroscopy in the picosecond to millisecond time range. We obtained a spectroscopic signature of the heme flattening upon O2 dissociation. The heme distortion is immediately (<1 ps) released after O2 dissociation to produce a relaxed state. This heme conformational change occurs with different proportions depending on diatomics as follows: CO < NO < O2. Our time-resolved data demonstrate that the primary structural event of allostery is the heme distortion in the Ct H-NOX sensor, contrastingly with hemoglobin and the human NO receptor, in which the primary structural events are respectively the motion of the proximal histidine and the rupture of the iron-histidine bond.

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Section: Introductionmentioning

confidence: 99%

Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium

et al. 2021

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“…NO signals dispersal of bacterial biofilms by interacting with enzymes that affect intracellular concentrations of bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP) (Williams and Boon, 2019). The molecular mechanism was recently characterised in some species of bacteria, including P. aeruginosa, Nitrosomonas europaea, and Shewanella oneidensis (Hossain and Boon, 2017;Hossain et al, 2017;Nisbett et al, 2019). Interaction of NO with NO-sensitive enzymes stimulates the activity of phosphodiesterases (PDEs), which degrade c-di-GMP and signal biofilm dispersal (McDougald et al, 2011).…”

Section: Nitric Oxidementioning

confidence: 99%

Combination Therapies for Biofilm Inhibition and Eradication: A Comparative Review of Laboratory and Preclinical Studies

Hawas

Verderosa

Totsika

2022

Front. Cell. Infect. Microbiol.

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Microbial biofilms are becoming increasingly difficult to treat in the medical setting due to their intrinsic resistance to antibiotics. To combat this, several biofilm dispersal agents are currently being developed as treatments for biofilm infections. Combining biofilm dispersal agents with antibiotics is emerging as a promising strategy to simultaneously disperse and eradicate biofilms or, in some cases, even inhibit biofilm formation. Here we review studies that have investigated the anti-biofilm activity of some well-studied biofilm dispersal agents (e.g., quorum sensing inhibitors, nitric oxide/nitroxides, antimicrobial peptides/amino acids) in combination with antibiotics from various classes. This review aims to directly compare the efficacy of different combination strategies against microbial biofilms and highlight synergistic treatments that warrant further investigation. By comparing across studies that use different measures of efficacy, we can conclude that treating biofilms in vitro and, in some limited cases in vivo, with a combination of an anti-biofilm agent and an antibiotic, appears overall more effective than treating with either compound alone. The review identifies the most promising combination therapies currently under development as biofilm inhibition and eradication therapies.

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“…[15a,85] Recently, NosP domain proteins have been identified as a novel NO-binding signal protein independent of H-NOX proteins in a number of bacteria, including P. aeruginosa, V. cholerae, and S. oneidensis (Figure 3). [83,87,88] Similar to H-NOX proteins, NosP proteins are also encoded by the genes in the same operon for proteins that are functionally associated with c-di-GMP metabolism. [15b] In addition to regulating biofilm formation and dispersion, both H-NOX and NosP NO signaling systems have been implicated in other biological processes such as quorum sensing and symbiosis in Vibrio species.…”

Section: Nitrite and No Signaling In Bacteriamentioning

confidence: 99%

“…Recently, NosP domain proteins have been identified as a novel NO‐binding signal protein independent of H‐NOX proteins in a number of bacteria, including P. aeruginosa , V. cholerae , and S. oneidensis (Figure 3). [ 83,87,88 ] Similar to H‐NOX proteins, NosP proteins are also encoded by the genes in the same operon for proteins that are functionally associated with c‐di‐GMP metabolism. [ 15b ]…”

Section: Nitrite and No Signaling In Bacteriamentioning

confidence: 99%

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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NosP Signaling Modulates the NO/H-NOX-Mediated Multicomponent c-Di-GMP Network and Biofilm Formation in Shewanella oneidensis

Cited by 21 publications

References 49 publications

Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium

Ultrafast dynamics of heme distortion in the O2-sensor of a thermophilic anaerobe bacterium

Combination Therapies for Biofilm Inhibition and Eradication: A Comparative Review of Laboratory and Preclinical Studies

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

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