Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition
The potency and indiscriminate nature of formaldehyde reactivity upon biological molecules make it a universal stressor. However, some organisms such as <i>Methylorubrum extorquens</i> possess means to rapidly and effectively mitigate formaldehyde-induced damage. EfgA is a recently ident...
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MDPI AG
2021-02-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/9/2/347 |
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| author | Jannell V. Bazurto Siavash Riazi Simon D’Alton Daniel E. Deatherage Eric L. Bruger Jeffrey E. Barrick Christopher J. Marx |
| author_facet | Jannell V. Bazurto Siavash Riazi Simon D’Alton Daniel E. Deatherage Eric L. Bruger Jeffrey E. Barrick Christopher J. Marx |
| author_sort | Jannell V. Bazurto |
| collection | DOAJ |
| description | The potency and indiscriminate nature of formaldehyde reactivity upon biological molecules make it a universal stressor. However, some organisms such as <i>Methylorubrum extorquens</i> possess means to rapidly and effectively mitigate formaldehyde-induced damage. EfgA is a recently identified formaldehyde sensor predicted to halt translation in response to elevated formaldehyde as a means to protect cells. Herein, we investigate growth and changes in gene expression to understand how <i>M. extorquens</i> responds to formaldehyde with and without the EfgA-formaldehyde-mediated translational response, and how this mechanism compares to antibiotic-mediated translation inhibition. These distinct mechanisms of translation inhibition have notable differences: they each involve different specific players and in addition, formaldehyde also acts as a general, multi-target stressor and a potential carbon source. We present findings demonstrating that in addition to its characterized impact on translation, functional EfgA allows for a rapid and robust transcriptional response to formaldehyde and that removal of EfgA leads to heightened proteotoxic and genotoxic stress in the presence of increased formaldehyde levels. We also found that many downstream consequences of translation inhibition were shared by EfgA-formaldehyde- and kanamycin-mediated translation inhibition. Our work uncovered additional layers of regulatory control enacted by functional EfgA upon experiencing formaldehyde stress, and further demonstrated the importance this protein plays at both transcriptional and translational levels in this model methylotroph. |
| first_indexed | 2024-03-09T04:53:21Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T04:53:21Z |
| publishDate | 2021-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-bc81e69b0cf24fd18a434e5ec7a643b42023-12-03T13:09:04ZengMDPI AGMicroorganisms2076-26072021-02-019234710.3390/microorganisms9020347Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational InhibitionJannell V. Bazurto0Siavash Riazi1Simon D’Alton2Daniel E. Deatherage3Eric L. Bruger4Jeffrey E. Barrick5Christopher J. Marx6Department of Biological Sciences, University of Idaho, Moscow, ID 83844, USADepartment of Biological Sciences, University of Idaho, Moscow, ID 83844, USACenter for Systems and Synthetic Biology, Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USACenter for Systems and Synthetic Biology, Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USADepartment of Biological Sciences, University of Idaho, Moscow, ID 83844, USACenter for Systems and Synthetic Biology, Department of Molecular Biosciences, The University of Texas at Austin, Austin, TX 78712, USADepartment of Biological Sciences, University of Idaho, Moscow, ID 83844, USAThe potency and indiscriminate nature of formaldehyde reactivity upon biological molecules make it a universal stressor. However, some organisms such as <i>Methylorubrum extorquens</i> possess means to rapidly and effectively mitigate formaldehyde-induced damage. EfgA is a recently identified formaldehyde sensor predicted to halt translation in response to elevated formaldehyde as a means to protect cells. Herein, we investigate growth and changes in gene expression to understand how <i>M. extorquens</i> responds to formaldehyde with and without the EfgA-formaldehyde-mediated translational response, and how this mechanism compares to antibiotic-mediated translation inhibition. These distinct mechanisms of translation inhibition have notable differences: they each involve different specific players and in addition, formaldehyde also acts as a general, multi-target stressor and a potential carbon source. We present findings demonstrating that in addition to its characterized impact on translation, functional EfgA allows for a rapid and robust transcriptional response to formaldehyde and that removal of EfgA leads to heightened proteotoxic and genotoxic stress in the presence of increased formaldehyde levels. We also found that many downstream consequences of translation inhibition were shared by EfgA-formaldehyde- and kanamycin-mediated translation inhibition. Our work uncovered additional layers of regulatory control enacted by functional EfgA upon experiencing formaldehyde stress, and further demonstrated the importance this protein plays at both transcriptional and translational levels in this model methylotroph.https://www.mdpi.com/2076-2607/9/2/347formaldehydestress responsetranslation inhibitionkanamycinmethylotrophyenhanced formaldehyde growth EfgA |
| spellingShingle | Jannell V. Bazurto Siavash Riazi Simon D’Alton Daniel E. Deatherage Eric L. Bruger Jeffrey E. Barrick Christopher J. Marx Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition Microorganisms formaldehyde stress response translation inhibition kanamycin methylotrophy enhanced formaldehyde growth EfgA |
| title | Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition |
| title_full | Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition |
| title_fullStr | Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition |
| title_full_unstemmed | Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition |
| title_short | Global Transcriptional Response of <i>Methylorubrum extorquens</i> to Formaldehyde Stress Expands the Role of EfgA and Is Distinct from Antibiotic Translational Inhibition |
| title_sort | global transcriptional response of i methylorubrum extorquens i to formaldehyde stress expands the role of efga and is distinct from antibiotic translational inhibition |
| topic | formaldehyde stress response translation inhibition kanamycin methylotrophy enhanced formaldehyde growth EfgA |
| url | https://www.mdpi.com/2076-2607/9/2/347 |
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