Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights
Abstract Background The halophilic bacterium Halomonas elongata is an industrially important strain for ectoine production, with high value and intense research focus. While existing studies primarily delve into the adaptive mechanisms of this bacterium under fixed salt concentrations, there is a no...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-03-01
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| Series: | Microbial Cell Factories |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12934-024-02358-5 |
| _version_ | 1797246944738803712 |
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| author | Junxiong Yu Yue Zhang Hao Liu Yuxuan Liu Ali Mohsin Zebo Liu Yanning Zheng Jianmin Xing Jing Han Yingping Zhuang Meijin Guo Zejian Wang |
| author_facet | Junxiong Yu Yue Zhang Hao Liu Yuxuan Liu Ali Mohsin Zebo Liu Yanning Zheng Jianmin Xing Jing Han Yingping Zhuang Meijin Guo Zejian Wang |
| author_sort | Junxiong Yu |
| collection | DOAJ |
| description | Abstract Background The halophilic bacterium Halomonas elongata is an industrially important strain for ectoine production, with high value and intense research focus. While existing studies primarily delve into the adaptive mechanisms of this bacterium under fixed salt concentrations, there is a notable dearth of attention regarding its response to fluctuating saline environments. Consequently, the stress response of H. elongata to salt shock remains inadequately understood. Results This study investigated the stress response mechanism of H. elongata when exposed to NaCl shock at short- and long-time scales. Results showed that NaCl shock induced two major stresses, namely osmotic stress and oxidative stress. In response to the former, within the cell’s tolerable range (1–8% NaCl shock), H. elongata urgently balanced the surging osmotic pressure by uptaking sodium and potassium ions and augmenting intracellular amino acid pools, particularly glutamate and glutamine. However, ectoine content started to increase until 20 min post-shock, rapidly becoming the dominant osmoprotectant, and reaching the maximum productivity (1450 ± 99 mg/L/h). Transcriptomic data also confirmed the delayed response in ectoine biosynthesis, and we speculate that this might be attributed to an intracellular energy crisis caused by NaCl shock. In response to oxidative stress, transcription factor cysB was significantly upregulated, positively regulating the sulfur metabolism and cysteine biosynthesis. Furthermore, the upregulation of the crucial peroxidase gene (HELO_RS18165) and the simultaneous enhancement of peroxidase (POD) and catalase (CAT) activities collectively constitute the antioxidant defense in H. elongata following shock. When exceeding the tolerance threshold of H. elongata (1–13% NaCl shock), the sustained compromised energy status, resulting from the pronounced inhibition of the respiratory chain and ATP synthase, may be a crucial factor leading to the stagnation of both cell growth and ectoine biosynthesis. Conclusions This study conducted a comprehensive analysis of H. elongata’s stress response to NaCl shock at multiple scales. It extends the understanding of stress response of halophilic bacteria to NaCl shock and provides promising theoretical insights to guide future improvements in optimizing industrial ectoine production. |
| first_indexed | 2024-04-24T19:50:51Z |
| format | Article |
| id | doaj.art-8fc288dfbbd245bea2b734a59069c993 |
| institution | Directory Open Access Journal |
| issn | 1475-2859 |
| language | English |
| last_indexed | 2024-04-24T19:50:51Z |
| publishDate | 2024-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbial Cell Factories |
| spelling | doaj.art-8fc288dfbbd245bea2b734a59069c9932024-03-24T12:38:01ZengBMCMicrobial Cell Factories1475-28592024-03-0123111910.1186/s12934-024-02358-5Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insightsJunxiong Yu0Yue Zhang1Hao Liu2Yuxuan Liu3Ali Mohsin4Zebo Liu5Yanning Zheng6Jianmin Xing7Jing Han8Yingping Zhuang9Meijin Guo10Zejian Wang11State Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyDepartment of Chemical Engineering for Energy Resources, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of SciencesInstitute of Process Engineering, Chinese Academy of SciencesState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of SciencesState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyState Key Laboratory of Bioreactor Engineering, East China University of Science and TechnologyAbstract Background The halophilic bacterium Halomonas elongata is an industrially important strain for ectoine production, with high value and intense research focus. While existing studies primarily delve into the adaptive mechanisms of this bacterium under fixed salt concentrations, there is a notable dearth of attention regarding its response to fluctuating saline environments. Consequently, the stress response of H. elongata to salt shock remains inadequately understood. Results This study investigated the stress response mechanism of H. elongata when exposed to NaCl shock at short- and long-time scales. Results showed that NaCl shock induced two major stresses, namely osmotic stress and oxidative stress. In response to the former, within the cell’s tolerable range (1–8% NaCl shock), H. elongata urgently balanced the surging osmotic pressure by uptaking sodium and potassium ions and augmenting intracellular amino acid pools, particularly glutamate and glutamine. However, ectoine content started to increase until 20 min post-shock, rapidly becoming the dominant osmoprotectant, and reaching the maximum productivity (1450 ± 99 mg/L/h). Transcriptomic data also confirmed the delayed response in ectoine biosynthesis, and we speculate that this might be attributed to an intracellular energy crisis caused by NaCl shock. In response to oxidative stress, transcription factor cysB was significantly upregulated, positively regulating the sulfur metabolism and cysteine biosynthesis. Furthermore, the upregulation of the crucial peroxidase gene (HELO_RS18165) and the simultaneous enhancement of peroxidase (POD) and catalase (CAT) activities collectively constitute the antioxidant defense in H. elongata following shock. When exceeding the tolerance threshold of H. elongata (1–13% NaCl shock), the sustained compromised energy status, resulting from the pronounced inhibition of the respiratory chain and ATP synthase, may be a crucial factor leading to the stagnation of both cell growth and ectoine biosynthesis. Conclusions This study conducted a comprehensive analysis of H. elongata’s stress response to NaCl shock at multiple scales. It extends the understanding of stress response of halophilic bacteria to NaCl shock and provides promising theoretical insights to guide future improvements in optimizing industrial ectoine production.https://doi.org/10.1186/s12934-024-02358-5Halomonas elongataEctoineNaCl shockStress responseOsmotic stressOxidative stress |
| spellingShingle | Junxiong Yu Yue Zhang Hao Liu Yuxuan Liu Ali Mohsin Zebo Liu Yanning Zheng Jianmin Xing Jing Han Yingping Zhuang Meijin Guo Zejian Wang Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights Microbial Cell Factories Halomonas elongata Ectoine NaCl shock Stress response Osmotic stress Oxidative stress |
| title | Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights |
| title_full | Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights |
| title_fullStr | Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights |
| title_full_unstemmed | Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights |
| title_short | Temporal dynamics of stress response in Halomonas elongata to NaCl shock: physiological, metabolomic, and transcriptomic insights |
| title_sort | temporal dynamics of stress response in halomonas elongata to nacl shock physiological metabolomic and transcriptomic insights |
| topic | Halomonas elongata Ectoine NaCl shock Stress response Osmotic stress Oxidative stress |
| url | https://doi.org/10.1186/s12934-024-02358-5 |
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