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Small RNAs Involved in Regulation of Nitrogen Metabolism

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  • Authors: Daniela Prasse1, Ruth A. Schmitz2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Christian-Albrechts-University Kiel, Institute of General Microbiology, D-24118 Kiel, Germany; 2: Christian-Albrechts-University Kiel, Institute of General Microbiology, D-24118 Kiel, Germany; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0018-2018
  • Received 12 January 2018 Accepted 25 April 2018 Published 20 July 2018
  • Ruth A. Schmitz, [email protected]
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  • Abstract:

    Global (metabolic) regulatory networks allow microorganisms to survive periods of nitrogen starvation or general nutrient stress. Uptake and utilization of various nitrogen sources are thus commonly tightly regulated in ( and ) in response to available nitrogen sources. Those well-studied regulations occur mainly at the transcriptional and posttranslational level. Surprisingly, and in contrast to their involvement in most other stress responses, small RNAs (sRNAs) involved in the response to environmental nitrogen fluctuations are only rarely reported. In addition to sRNAs indirectly affecting nitrogen metabolism, only recently it was demonstrated that three sRNAs were directly involved in regulation of nitrogen metabolism in response to changes in available nitrogen sources. All three -acting sRNAs are under direct transcriptional control of global nitrogen regulators and affect expression of components of nitrogen metabolism (glutamine synthetase, nitrogenase, and PII-like proteins) by either masking the ribosome binding site and thus inhibiting translation initiation or stabilizing the respective target mRNAs. Most likely, there are many more sRNAs and other types of noncoding RNAs, e.g., riboswitches, involved in the regulation of nitrogen metabolism in that remain to be uncovered. The present review summarizes the current knowledge on sRNAs involved in nitrogen metabolism and their biological functions and targets.

  • Citation: Prasse D, Schmitz R. 2018. Small RNAs Involved in Regulation of Nitrogen Metabolism. Microbiol Spectrum 6(4):RWR-0018-2018. doi:10.1128/microbiolspec.RWR-0018-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0018-2018
2018-07-20
2018-10-20

Abstract:

Global (metabolic) regulatory networks allow microorganisms to survive periods of nitrogen starvation or general nutrient stress. Uptake and utilization of various nitrogen sources are thus commonly tightly regulated in ( and ) in response to available nitrogen sources. Those well-studied regulations occur mainly at the transcriptional and posttranslational level. Surprisingly, and in contrast to their involvement in most other stress responses, small RNAs (sRNAs) involved in the response to environmental nitrogen fluctuations are only rarely reported. In addition to sRNAs indirectly affecting nitrogen metabolism, only recently it was demonstrated that three sRNAs were directly involved in regulation of nitrogen metabolism in response to changes in available nitrogen sources. All three -acting sRNAs are under direct transcriptional control of global nitrogen regulators and affect expression of components of nitrogen metabolism (glutamine synthetase, nitrogenase, and PII-like proteins) by either masking the ribosome binding site and thus inhibiting translation initiation or stabilizing the respective target mRNAs. Most likely, there are many more sRNAs and other types of noncoding RNAs, e.g., riboswitches, involved in the regulation of nitrogen metabolism in that remain to be uncovered. The present review summarizes the current knowledge on sRNAs involved in nitrogen metabolism and their biological functions and targets.

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Figures

Image of FIGURE 1
FIGURE 1

Nitrogen metabolism and regulation. The main components of nitrogen metabolism are depicted in a simplified way. Under nitrogen limitation (left), the GS with high binding affinity to ammonium (NH ) is activated. The remaining NH is actively transferred by ammonia transporters (AmtB) into the cell and dinitrogen (N) directly reduced into ammonium by the key enzyme nitrogenase. Subsequently, NH is assimilated by the GS and the GOGAT system. Under nitrogen sufficiency (right), the GS is inhibited and ammonia diffuses over the cytoplasm membrane into the cell, which can be directly assimilated by the glutamate dehydrogenase (low affinity). PII-like proteins are involved in most regulatory ways, sensing the current nitrogen status within the cell and forwarding the respective signal to GS, inducing reversible deactivation of GS by covalent modifications or direct interactions with proteins in response to the nitrogen availability, but also to nitrogenase and ammonia transporters (for details, see reference 9 ).

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0018-2018
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Image of FIGURE 2
FIGURE 2

Visualization of microorganisms for which currently known sRNAs are directly or indirectly involved in nitrogen metabolism and their phylogenetic distribution. Organisms belonging to the two different phylogenetic domains of and are colored and single organisms are exemplarily indicated. Each organism is depicted with its attendant sRNAs. sp. image obtained with confocal microscopy; , light microscopy; , fluorescence phase-contrast microscopy; and and , scanning electron microscopy.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0018-2018
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Image of FIGURE 3
FIGURE 3

Functional mechanisms of three sRNAs directly involved in regulation of nitrogen fixation. (A) The sRNA is a central regulatory component within the regulatory network of nitrogen fixation in strain Gö1. It was shown that sRNA acts on several target mRNAs by either stabilizing the mRNA by direct binding (in case of , , and operon) or repressing translation initiation by blocking the RBS (in case of ). In addition, sRNA-mediated regulation allows feedforward regulation of expression via mRNA stabilization. (B) In A1501, sRNA NfiS targets mRNA (possibly multiple times) and enhances transcript stability, very similar to sRNA in , which also targets and operon, possibly at multiple regions. (C) NsiR4 from 6803 interacts with mRNA, which encodes GS-inactivation factor 7, and blocks translation initiation by targeting the 5′ UTR of , consequently leading to a positive effect on GS activity under nitrogen limitation. This mode of action is very similar to that of sRNA, which targets the 5′ UTR of the transcript as well and represses translation initiation. post-tcript, posttranscriptional.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0018-2018
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Tables

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TABLE 1

sRNAs involved in nitrogen metabolism and their specific characteristics

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0018-2018

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