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The CRP-like transcriptional regulator MrpC curbs c-di-GMP and 3’, 3’ cGAMP nucleotide levels during development in Myxococcus xanthus

Sofya Kuzmich, Patrick Blumenkamp, Doreen Meier, Alexander Goesmann, Anke Becker, View ORCID ProfileLotte Søgaard-Andersen
doi: https://doi.org/10.1101/2021.10.14.464357
Sofya Kuzmich
1Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Str. 10, 35043 Marburg, Germany
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Patrick Blumenkamp
2Systems Biology and Bioinformatics, Justus Liebig University Giessen, Heinrich-Buff-Ring Str. 58, 35392 Gießen, Germany
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Doreen Meier
3Center for Synthetic Microbiology (SYNMIKRO), Philipps Universität Marburg Karl-von-Frisch-Str. 14, 35043 Marburg, Germany
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Alexander Goesmann
2Systems Biology and Bioinformatics, Justus Liebig University Giessen, Heinrich-Buff-Ring Str. 58, 35392 Gießen, Germany
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Anke Becker
3Center for Synthetic Microbiology (SYNMIKRO), Philipps Universität Marburg Karl-von-Frisch-Str. 14, 35043 Marburg, Germany
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Lotte Søgaard-Andersen
1Department of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Str. 10, 35043 Marburg, Germany
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  • ORCID record for Lotte Søgaard-Andersen
  • For correspondence: sogaard@mpi-marburg.mpg.de
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Abstract

Myxococcus xanthus has a nutrient-regulated biphasic lifecycle forming predatory swarms in the presence of nutrients and spore-filled fruiting bodies in the absence of nutrients. The second messenger c-di-GMP is essential during both stages of the lifecycle; however, different enzymes involved in c-di-GMP synthesis and degradation as well as several c-di-GMP receptors are important during distinct lifecycle stages. To address this stage specificity, we determined transcript levels using RNA-seq and transcription start sites using Cappable-seq during growth and development at a genome-wide scale. All 70 genes encoding c-di-GMP associated proteins were expressed, with 28 up-regulated and 10 down-regulated during development. In particular, the three genes encoding enzymatically active proteins with a stage-specific function were expressed stage-specifically. By combining operon mapping with published ChIP-seq data for MrpC (Robinson et al., 2014), the CRP-like master regulator of development, we identified nine developmentally regulated genes as regulated by MrpC. In particular, MrpC directly represses expression of dmxB, which encodes the diguanylate cyclase DmxB that is essential for development and responsible for the c-di-GMP increase during development. Moreover, MrpC directly activates transcription of pmxA, which encodes a bifunctional phosphodiesterase that degrades c-di-GMP and 3’, 3’ cGAMP in vitro and is essential for development. Thereby, MrpC regulates and curbs the cellular pools of c-di-GMP and 3’, 3’ cGAMP during development. We conclude that temporal regulation of the synthesis of proteins involved in c-di-GMP metabolism contributes to c-di-GMP signaling specificity. MrpC is important for this regulation, thereby being a key regulator of developmental cyclic di-nucleotide metabolism in M. xanthus.

Importance The second messenger c-di-GMP is important during both stages of the nutrient-regulated biphasic lifecycle of Myxococcus xanthus with the formation of predatory swarms in the presence of nutrients and spore-filled fruiting bodies in the absence of nutrients. However, different enzymes involved in c-di-GMP synthesis and degradation are important during distinct lifecycle stages. Here, we show that the three genes encoding enzymatically active proteins with a stage-specific function are expressed stage-specifically. Moreover, we find that the master transcriptional regulator of development MrpC directly regulates expression of dmxB, which encodes the diguanylate cyclase DmxB that is essential for development, and of pmxA, which encodes a bifunctional phosphodiesterase that degrades c-di-GMP and 3’, 3’ cGAMP in vitro and is essential for development. We conclude that temporal regulation of the synthesis of proteins involved in c-di-GMP metabolism contributes to c-di-GMP signaling specificity, and that MrpC plays an important role in this regulation.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted October 14, 2021.
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The CRP-like transcriptional regulator MrpC curbs c-di-GMP and 3’, 3’ cGAMP nucleotide levels during development in Myxococcus xanthus
Sofya Kuzmich, Patrick Blumenkamp, Doreen Meier, Alexander Goesmann, Anke Becker, Lotte Søgaard-Andersen
bioRxiv 2021.10.14.464357; doi: https://doi.org/10.1101/2021.10.14.464357
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The CRP-like transcriptional regulator MrpC curbs c-di-GMP and 3’, 3’ cGAMP nucleotide levels during development in Myxococcus xanthus
Sofya Kuzmich, Patrick Blumenkamp, Doreen Meier, Alexander Goesmann, Anke Becker, Lotte Søgaard-Andersen
bioRxiv 2021.10.14.464357; doi: https://doi.org/10.1101/2021.10.14.464357

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