PDF(Pubmed)
Abstract：
BACKGROUND: Active hydrothermal vents create extreme conditions characterized by high temperatures, low pH levels, and elevated concentrations of heavy metals and other trace elements. These conditions support unique ecosystems where chemolithoautotrophs serve as primary producers. The steep temperature and pH gradients from the vent mouth to its periphery provide a wide range of microhabitats for these specialized microorganisms. However, their metabolic functions, adaptations in response to these gradients, and coping mechanisms under extreme conditions remain areas of limited knowledge. In this study, we conducted temperature gradient incubations of hydrothermal fluids from moderate (pH = 5.6) and extremely (pH = 2.2) acidic vents. Combining the DNA-stable isotope probing technique and subsequent metagenomics, we identified active chemolithoautotrophs under different temperature and pH conditions and analyzed their specific metabolic mechanisms.
RESULTS: We found that the carbon fixation activities of Nautiliales in vent fluids were significantly increased from 45 to 65 °C under moderately acidic condition, while their heat tolerance was reduced under extremely acidic conditions. In contrast, Campylobacterales actively fixed carbon under both moderately and extremely acidic conditions under 30 - 45 °C. Compared to Campylobacterales, Nautiliales were found to lack the Sox sulfur oxidation system and instead use NAD(H)-linked glutamate dehydrogenase to boost the reverse tricarboxylic acid (rTCA) cycle. Additionally, they exhibit a high genetic potential for high activity of cytochrome bd ubiquinol oxidase in oxygen respiration and hydrogen oxidation at high temperatures. In terms of high-temperature adaption, the rgy gene plays a critical role in Nautiliales by maintaining DNA stability at high temperature. Genes encoding proteins involved in proton export, including the membrane arm subunits of proton-pumping NADH: ubiquinone oxidoreductase, K+ accumulation, selective transport of charged molecules, permease regulation, and formation of the permeability barrier of bacterial outer membranes, play essential roles in enabling Campylobacterales to adapt to extremely acidic conditions.
CONCLUSIONS: Our study provides in-depth insights into how high temperature and low pH impact the metabolic processes of energy and main elements in chemolithoautotrophs living in hydrothermal ecosystems, as well as the mechanisms they use to adapt to the extreme hydrothermal conditions. Video Abstract.
RESULTS: We found that the carbon fixation activities of Nautiliales in vent fluids were significantly increased from 45 to 65 °C under moderately acidic condition, while their heat tolerance was reduced under extremely acidic conditions. In contrast, Campylobacterales actively fixed carbon under both moderately and extremely acidic conditions under 30 - 45 °C. Compared to Campylobacterales, Nautiliales were found to lack the Sox sulfur oxidation system and instead use NAD(H)-linked glutamate dehydrogenase to boost the reverse tricarboxylic acid (rTCA) cycle. Additionally, they exhibit a high genetic potential for high activity of cytochrome bd ubiquinol oxidase in oxygen respiration and hydrogen oxidation at high temperatures. In terms of high-temperature adaption, the rgy gene plays a critical role in Nautiliales by maintaining DNA stability at high temperature. Genes encoding proteins involved in proton export, including the membrane arm subunits of proton-pumping NADH: ubiquinone oxidoreductase, K+ accumulation, selective transport of charged molecules, permease regulation, and formation of the permeability barrier of bacterial outer membranes, play essential roles in enabling Campylobacterales to adapt to extremely acidic conditions.
CONCLUSIONS: Our study provides in-depth insights into how high temperature and low pH impact the metabolic processes of energy and main elements in chemolithoautotrophs living in hydrothermal ecosystems, as well as the mechanisms they use to adapt to the extreme hydrothermal conditions. Video Abstract.
摘要：
背景：活跃的热液喷口创造了以高温为特征的极端条件，低pH值,以及重金属和其他微量元素的浓度升高。这些条件支持独特的生态系统，其中化学自养生物是初级生产者。从排气口到其周围的陡峭温度和pH梯度为这些专门的微生物提供了广泛的微生境。然而,它们的代谢功能，适应这些梯度，极端条件下的应对机制仍然是知识有限的领域。在这项研究中,我们对来自中等（pH=5.6）和极（pH=2.2）酸性喷口的热液进行了温度梯度孵育。结合DNA稳定同位素探测技术和随后的宏基因组学，我们在不同的温度和pH条件下鉴定了活跃的化学自养生物，并分析了其特定的代谢机制。
结果：我们发现，在中等酸性条件下，从45到65°C，排气液中的鹦鹉鱼的碳固定活性显着增加，而它们的耐热性在极端酸性条件下降低。相比之下,在30-45°C的中等和极酸性条件下，弯曲杆菌主动固定碳。与弯曲杆菌相比，发现鹦鹉缺乏Sox硫氧化系统，而是使用NAD（H）连接的谷氨酸脱氢酶来促进反向三羧酸（rTCA）循环。此外,它们在高温下的氧呼吸和氢氧化中表现出细胞色素bd泛醇氧化酶高活性的高遗传潜力。在高温适应方面，rgy基因通过在高温下保持DNA稳定性在鹦鹉中发挥关键作用。编码参与质子输出的蛋白质的基因，包括质子泵NADH的膜臂亚基：泛醌氧化还原酶，K+积累,带电分子的选择性运输，渗透酶调节，和细菌外膜渗透屏障的形成，在使弯曲杆菌适应极端酸性条件方面发挥重要作用。
结论：我们的研究深入了解了高温和低pH如何影响生活在热液生态系统中的化学自养生物中的能量和主要元素的代谢过程，以及他们用来适应极端热液条件的机制。视频摘要。
结果：我们发现，在中等酸性条件下，从45到65°C，排气液中的鹦鹉鱼的碳固定活性显着增加，而它们的耐热性在极端酸性条件下降低。相比之下,在30-45°C的中等和极酸性条件下，弯曲杆菌主动固定碳。与弯曲杆菌相比，发现鹦鹉缺乏Sox硫氧化系统，而是使用NAD（H）连接的谷氨酸脱氢酶来促进反向三羧酸（rTCA）循环。此外,它们在高温下的氧呼吸和氢氧化中表现出细胞色素bd泛醇氧化酶高活性的高遗传潜力。在高温适应方面，rgy基因通过在高温下保持DNA稳定性在鹦鹉中发挥关键作用。编码参与质子输出的蛋白质的基因，包括质子泵NADH的膜臂亚基：泛醌氧化还原酶，K+积累,带电分子的选择性运输，渗透酶调节，和细菌外膜渗透屏障的形成，在使弯曲杆菌适应极端酸性条件方面发挥重要作用。
结论：我们的研究深入了解了高温和低pH如何影响生活在热液生态系统中的化学自养生物中的能量和主要元素的代谢过程，以及他们用来适应极端热液条件的机制。视频摘要。
