Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S
<i>Listeria monocytogenes</i> is a foodborne pathogen frequently exposed to oxidative stress in diverse environmental conditions. Cyclic di-AMP (c-di-AMP) is a second messenger that plays a key role in stress resistance. This study investigates the role of <i>pdeA</i> (degrad...
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2025-06-01
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| author | Mahide Muge Yilmaz Topcam Dimitrios P. Balagiannis Kimon Andreas G. Karatzas |
| author_facet | Mahide Muge Yilmaz Topcam Dimitrios P. Balagiannis Kimon Andreas G. Karatzas |
| author_sort | Mahide Muge Yilmaz Topcam |
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| description | <i>Listeria monocytogenes</i> is a foodborne pathogen frequently exposed to oxidative stress in diverse environmental conditions. Cyclic di-AMP (c-di-AMP) is a second messenger that plays a key role in stress resistance. This study investigates the role of <i>pdeA</i> (degrades c-di-AMP) and how c-di-AMP accumulation affects catalase activity and oxidative stress response and gene expression. Survival and catalase activity assays were conducted under oxidative stress, and c-di-AMP levels were quantified in <i>L. monocytogenes</i> 10403S under aerobic, anaerobic, and L-cysteine-supplemented conditions. Δ<i>pdeA</i>, which accumulates c-di-AMP, exhibited greater sensitivity to oxidative stress (4.6 log reduction for the wild type (WT) vs 7.34 log reduction for Δ<i>pdeA</i> at 10 h) and lower catalase activity than the WT in the early stationary phase. However, in the late stationary phase, while the catalase activity levels of Δ<i>pdeA</i> remained stable (~6.33 cm foam height), it became resistant to oxidative stress (5.85 log reduction). These findings indicate that <i>pdeA</i> contributes to catalase activity in <i>L. monocytogenes</i>. Transcriptomic analysis revealed differential expression of pathways mainly including pentose phosphate pathway, carbon metabolism, O-antigen nucleotide sugar biosynthesis and ABC transporters in Δ<i>pdeA</i> compared to WT. Our transcriptomic data provided promising insights into the molecular mechanisms underlying c-di-AMP regulation, which may enhance stress resistance. Moreover, oxidative stress led to increased intracellular c-di-AMP levels. Under L-cysteine supplementation, catalase activity levels in WT were similar to Δ<i>pdeA</i> (~1.86 cm foam height for both), but the latter showed enhanced oxidative stress resistance and c-di-AMP levels. Anaerobic conditions also elevated c-di-AMP levels in WT and Δ<i>pdeA</i> but resulted in greater oxidative stress sensitivity. Understanding these regulatory mechanisms provides valuable insights into oxidative stress resistance, with potential implications for food safety and pathogen control. |
| format | Article |
| id | doaj-art-619e1eb2c8a940c7aa5bb0053f90fa02 |
| institution | Matheson Library |
| issn | 2076-2607 |
| language | English |
| publishDate | 2025-06-01 |
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| spelling | doaj-art-619e1eb2c8a940c7aa5bb0053f90fa022025-06-25T14:12:48ZengMDPI AGMicroorganisms2076-26072025-06-01136140010.3390/microorganisms13061400Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403SMahide Muge Yilmaz Topcam0Dimitrios P. Balagiannis1Kimon Andreas G. Karatzas2Department of Food and Nutritional Sciences, School of Chemistry, Food and Pharmacy, University of Reading, Reading RG6 6AD, UKDepartment of Food and Nutritional Sciences, School of Chemistry, Food and Pharmacy, University of Reading, Reading RG6 6AD, UKDepartment of Food and Nutritional Sciences, School of Chemistry, Food and Pharmacy, University of Reading, Reading RG6 6AD, UK<i>Listeria monocytogenes</i> is a foodborne pathogen frequently exposed to oxidative stress in diverse environmental conditions. Cyclic di-AMP (c-di-AMP) is a second messenger that plays a key role in stress resistance. This study investigates the role of <i>pdeA</i> (degrades c-di-AMP) and how c-di-AMP accumulation affects catalase activity and oxidative stress response and gene expression. Survival and catalase activity assays were conducted under oxidative stress, and c-di-AMP levels were quantified in <i>L. monocytogenes</i> 10403S under aerobic, anaerobic, and L-cysteine-supplemented conditions. Δ<i>pdeA</i>, which accumulates c-di-AMP, exhibited greater sensitivity to oxidative stress (4.6 log reduction for the wild type (WT) vs 7.34 log reduction for Δ<i>pdeA</i> at 10 h) and lower catalase activity than the WT in the early stationary phase. However, in the late stationary phase, while the catalase activity levels of Δ<i>pdeA</i> remained stable (~6.33 cm foam height), it became resistant to oxidative stress (5.85 log reduction). These findings indicate that <i>pdeA</i> contributes to catalase activity in <i>L. monocytogenes</i>. Transcriptomic analysis revealed differential expression of pathways mainly including pentose phosphate pathway, carbon metabolism, O-antigen nucleotide sugar biosynthesis and ABC transporters in Δ<i>pdeA</i> compared to WT. Our transcriptomic data provided promising insights into the molecular mechanisms underlying c-di-AMP regulation, which may enhance stress resistance. Moreover, oxidative stress led to increased intracellular c-di-AMP levels. Under L-cysteine supplementation, catalase activity levels in WT were similar to Δ<i>pdeA</i> (~1.86 cm foam height for both), but the latter showed enhanced oxidative stress resistance and c-di-AMP levels. Anaerobic conditions also elevated c-di-AMP levels in WT and Δ<i>pdeA</i> but resulted in greater oxidative stress sensitivity. Understanding these regulatory mechanisms provides valuable insights into oxidative stress resistance, with potential implications for food safety and pathogen control.https://www.mdpi.com/2076-2607/13/6/1400<i>Listeria monocytogenes</i>second messengerc-di-AMP accumulationphosphodiesteraseoxidative stress resistancecatalase activity |
| spellingShingle | Mahide Muge Yilmaz Topcam Dimitrios P. Balagiannis Kimon Andreas G. Karatzas Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S Microorganisms <i>Listeria monocytogenes</i> second messenger c-di-AMP accumulation phosphodiesterase oxidative stress resistance catalase activity |
| title | Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S |
| title_full | Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S |
| title_fullStr | Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S |
| title_full_unstemmed | Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S |
| title_short | Impact of c-di-AMP Accumulation, L-cysteine, and Oxygen on Catalase Activity and Oxidative Stress Resistance of <i>Listeria monocytogenes</i> 10403S |
| title_sort | impact of c di amp accumulation l cysteine and oxygen on catalase activity and oxidative stress resistance of i listeria monocytogenes i 10403s |
| topic | <i>Listeria monocytogenes</i> second messenger c-di-AMP accumulation phosphodiesterase oxidative stress resistance catalase activity |
| url | https://www.mdpi.com/2076-2607/13/6/1400 |
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