The Anaerobically Induced sRNA PaiI Affects Denitrification in Pseudomonas aeruginosa PA14

Tata, Muralidhar; Amman, Fabian; Pawar, Vinay; Wolfinger, Michael T.; Weiß, Siegfried; Häußler, Susanne; Bläsi, Udo

doi:10.3389/fmicb.2017.02312

Cited by 14 publications

(16 citation statements)

References 67 publications

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“…aeruginosa 14 (PA14) which seemed to be important for denitrification. However, overexpression of the sRNA did not affect levels of nitrite reductase, leading the authors to conclude that this sRNA was exerting an indirect effect on denitrification (23), in comparison to the sRNA described in this study.…”

Section: Discussioncontrasting

confidence: 56%

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions

Gaimster

Griffiths

Soriano-Laguna

et al. 2019

mBio

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Global atmospheric loading of the climate-active gas nitrous oxide (N2O) continues to increase. A significant proportion of anthropogenic N2O emissions arises from microbial transformation of nitrogen-based fertilizers during denitrification, making microbial N2O emissions a key target for greenhouse gas reduction strategies. The genetic, physiological, and environmental regulation of microbially mediated N2O flux is poorly understood and therefore represents a critical knowledge gap in the development of successful mitigation approaches. We have previously mapped the transcriptional landscape of the model soil-denitrifying bacterium Paracoccus denitrificans. Here, we show that a single bacterial small RNA (sRNA) can control the denitrification rate of P. denitrificans by stalling denitrification at nitrite reduction to limit production of downstream pathway intermediates and N2O emissions. Overexpression of sRNA-29 downregulates nitrite reductase and limits NO and N2O production by cells. RNA sequencing (RNA-seq) analysis revealed 53 genes that are controlled by sRNA-29, one of which is a previously uncharacterized GntR-type transcriptional regulator. Overexpression of this regulator phenocopies sRNA-29 overexpression and allows us to propose a model whereby sRNA-29 enhances levels of the regulator to repress denitrification under appropriate conditions. Our identification of a new regulatory pathway controlling the core denitrification pathway in bacteria highlights the current chasm in knowledge regarding genetic regulation of this pivotal biogeochemical process, which needs to be closed to support future biological and chemical N2O mitigation strategies. IMPORTANCE N2O is an important greenhouse gas and a major cause of ozone depletion. Denitrifying bacteria play vital roles in the production and consumption of N2O in many environments. Complete denitrification consists of the conversion of a soluble N-oxyanion, nitrate (NO3-), to an inert gaseous N-oxide, dinitrogen (N2). Incomplete denitrification can occur if conditions are prohibitive, for example, under conditions of low soil copper concentrations, leading to emission of N2O rather than N2. Although enzymatically well characterized, the genetic drivers that regulate denitrification in response to environmental and physiological cues are not fully understood. This study identified a new regulatory sRNA-based control mechanism for denitrification in the model denitrifying bacterium P. denitrificans. Overexpression of this sRNA slows the rate of denitrification. This report highlights that there are gaps in understanding the regulation of this important pathway which need to be filled if strategies for N2O mitigation can be rationally and carefully developed.

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Section: Discussioncontrasting

confidence: 56%

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions

Gaimster

Griffiths

Soriano-Laguna

et al. 2019

mBio

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“…The NarGHI complex is a typical molybdoenzyme, which reduces nitrate to nitrite in the initial step of the anaerobic growth process (Kraft et al, 2011). In P. aeruginosa, the switch from aerobic to anaerobic growth is controlled by Anr, a master regulator that responds to oxygen limitation (Tata et al, 2017).…”

Section: àmentioning

confidence: 99%

Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis

Wang

et al. 2021

Cell Reports

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“…Lastly, connections between sRNAs and nitrogen are not restricted to enterobacteria and many other examples have been reported in extremely diverse bacteria as well, including the sRNAs related to denitrification in Pseudomonas aeruginosa or Paracoccus denitrificans [70,71], the RoxS sRNA that responds to nitric oxide in firmicutes [72] and the sRNAs involved in the control of carbon-nitrogen balance in cyanobacteria [73].…”

Section: Discussionmentioning

confidence: 99%

Synthesis of the NarP response regulator of nitrate respiration inEscherichia coliis regulated at multiple levels by Hfq and small RNAs

Brosse

Walburger

Magalon

et al. 2021

Preprint

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Two-component systems (TCS) and small RNAs (sRNA) are widespread regulators that participate in the response and the adaptation of bacteria to their environments. They mostly act at the transcriptional and post-transcriptional levels, respectively, and can be found integrated in regulatory circuits, where TCSs control sRNAs transcription and/or sRNAs post-transcriptionally regulate TCSs synthesis.In response to nitrate and nitrite, the paralogous NarQ-NarP and NarX-NarL TCSs regulate the expression of genes involved in anaerobic respiration of these alternative electron acceptors. In addition to the previously reported repression of NarP synthesis by the SdsN137 sRNA, we show here that RprA, another Hfq-dependent sRNA, also negatively controls narP. Interestingly, the repression of narP by RprA actually relies on two independent controls. The first is via the direct pairing of the central region of RprA to the narP translation initiation region and presumably occurs at the translation initiation level. In contrast, the second control requires only the very 5’ end of the narP mRNA, which is targeted, most likely indirectly, by the full-length or the shorter, processed, form of RprA. In addition, our results raise the possibility of a direct role of Hfq in narP control, further illustrating the diversity of post-transcriptional regulation mechanisms in the synthesis of TCSs.

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The Anaerobically Induced sRNA PaiI Affects Denitrification in Pseudomonas aeruginosa PA14

Cited by 14 publications

References 67 publications

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions

Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis

Synthesis of the NarP response regulator of nitrate respiration inEscherichia coliis regulated at multiple levels by Hfq and small RNAs

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The Anaerobically Induced sRNA PaiI Affects Denitrification in Pseudomonas aeruginosa PA14

Cited by 14 publications

References 67 publications

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N 2 O Emissions

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N 2 O Emissions

Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis

Synthesis of the NarP response regulator of nitrate respiration inEscherichia coliis regulated at multiple levels by Hfq and small RNAs

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A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions

A Central Small RNA Regulatory Circuit Controlling Bacterial Denitrification and N ₂ O Emissions