State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, 130 Meilong Rd, Shanghai, 200237, China.
Department of Chemical Engineering for Energy Resources, East China University of Science and Technology, 130 Meilong Rd, Shanghai, 200237, China.
Microb Cell Fact. 2024 Mar 23;23(1):88. doi: 10.1186/s12934-024-02358-5.
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.
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.
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.
嗜盐菌 Halomonas elongata 是一种具有工业重要价值且备受关注的产胞外多胺菌株。尽管现有研究主要集中在该菌在固定盐浓度下的适应机制，但对其在波动盐环境中的响应却鲜有研究。因此，H. elongata 对盐冲击的应激反应仍未得到充分了解。
本研究从短期和长期两个时间尺度研究了 H. elongata 暴露于 NaCl 冲击时的应激反应机制。结果表明，NaCl 冲击引起了两种主要的应激，即渗透压应激和氧化应激。在细胞可耐受的范围内（1-8% NaCl 冲击），H. elongata 迅速摄取钠离子和钾离子并增加细胞内氨基酸库，特别是谷氨酸和谷氨酰胺，以平衡不断增加的渗透压。然而，胞外多胺的含量在冲击后 20 分钟开始增加，迅速成为主要的渗透压保护剂，并达到最大生产力（1450±99mg/L/h）。转录组数据也证实了胞外多胺生物合成的延迟反应，我们推测这可能是由于 NaCl 冲击引起的细胞内能量危机。针对氧化应激，转录因子 cysB 显著上调，正向调节硫代谢和半胱氨酸生物合成。此外，关键过氧化物酶基因（HELO_RS18165）的上调以及过氧化物酶（POD）和过氧化氢酶（CAT）活性的同时增强，共同构成了 H. elongata 冲击后的抗氧化防御。当超过 H. elongata 的耐受阈值（1-13% NaCl 冲击）时，呼吸链和 ATP 合酶显著抑制导致的持续受损的能量状态可能是导致细胞生长和胞外多胺生物合成停滞的关键因素。
本研究从多个尺度综合分析了 H. elongata 对 NaCl 冲击的应激反应。它扩展了对嗜盐菌对 NaCl 冲击的应激反应的理解，为指导未来优化工业胞外多胺生产提供了有前景的理论见解。
