Zhao Weishu, Ma Xiaopan, Liu Xiaoxia, Jian Huahua, Zhang Yu, Xiao Xiang
State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
State Key Laboratory of Ocean Engineering, Shanghai Jiao Tong University, Shanghai, China.
Front Microbiol. 2020 Sep 10;11:2081. doi: 10.3389/fmicb.2020.02081. eCollection 2020.
Hyperthermophiles, living in environments above 80°C and usually coupling with multi-extreme environmental stresses, have drawn great attention due to their application potential in biotechnology and being the primitive extant forms of life. Studies on their survival and adaptation mechanisms have extended our understanding on how lives thrive under extreme conditions. During these studies, the "cross-stress" behavior in various organisms has been observed between the extreme high temperature and other environmental stresses. Despite the broad observation, the global view of the cross-stress behavior remains unclear in hyperthermophiles, leaving a knowledge gap in our understanding of extreme adaptation. In this study, we performed a global quantitative proteomic analysis under extreme temperatures, pH, hydrostatic pressure (HP), and salinity on an archaeal strain, A501, which has outstanding growth capability on a wide range of temperatures (50-100°C), pH (4-9), and HPs (0.1-70 MPa), but a narrow range of NaCl (1.0-5.0 %, w/v). The proteomic analysis (79.8% genome coverage) demonstrated that approximately 61.5% of the significant differentially expressed proteins (DEPs) responded to multiple stresses. The responses to most of the tested stresses were closely correlated, except the responses to high salinity and low temperature. The top three enriched universal responding processes include the biosynthesis and protection of macromolecules, biosynthesis and metabolism of amino acids, ion transport, and binding activities. In addition, this study also revealed that the specific dual-stress responding processes, such as the membrane lipids for both cold and HP stresses and the signal transduction for both hyperosmotic and heat stresses, as well as the sodium-dependent energetic processes might be the limiting factor of the growth range in salinity. The present study is the first to examine the global cross-stress responses in a piezophilic hyperthermophile at the proteomic level. Our findings provide direct evidences of the cross-stress adaptation strategy (33.5% of coding-genes) to multiple stresses and highlight the specific and unique responding processes (0.22-0.63% of coding genes for each) to extreme temperature, pH, salinity, and pressure, which are highly relevant to the fields of evolutionary biology as well as next generation industrial biotechnology (NGIB).
嗜热菌生活在80°C以上的环境中，通常伴随着多种极端环境压力，由于其在生物技术中的应用潜力以及作为现存原始生命形式而备受关注。对其生存和适应机制的研究扩展了我们对生命如何在极端条件下蓬勃发展的理解。在这些研究中，已观察到各种生物体在极端高温和其他环境压力之间存在“交叉应激”行为。尽管有广泛的观察，但嗜热菌中交叉应激行为的全局视图仍不清楚，这在我们对极端适应的理解上留下了知识空白。在本研究中，我们对一株古菌菌株A501在极端温度、pH值、静水压力（HP）和盐度条件下进行了全局定量蛋白质组分析。该菌株在广泛的温度范围（50-100°C）、pH值（4-9）和HP范围（0.1-70 MPa）具有出色的生长能力，但NaCl范围较窄（1.0-5.0%，w/v）。蛋白质组分析（基因组覆盖率79.8%）表明，约61.5%的显著差异表达蛋白（DEP）对多种应激作出反应。除了对高盐度和低温的反应外，对大多数测试应激的反应密切相关。富集程度最高的前三个通用反应过程包括大分子的生物合成和保护、氨基酸的生物合成和代谢、离子运输以及结合活性。此外，本研究还揭示了特定的双应激反应过程，如针对低温和HP应激的膜脂、针对高渗和热应激的信号转导以及钠依赖性能量过程可能是盐度生长范围的限制因素。本研究首次在蛋白质组水平上研究了嗜压嗜热菌中的全局交叉应激反应。我们的发现提供了交叉应激适应策略（占编码基因的33.5%）对多种应激的直接证据，并突出了针对极端温度、pH值、盐度和压力的特定且独特的反应过程（每个占编码基因的0.22-0.63%），这与进化生物学以及下一代工业生物技术（NGIB）领域高度相关。
