Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress.
Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress.
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DOI：
10.1128/aem.02988-20
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发表时间：
2021-05-11
影响因子：
4.4
通讯作者：
Siebers B
中科院分区：
文献类型：
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作者：
Benninghoff JC;Kuschmierz L;Zhou X;Albersmeier A;Pham TK;Busche T;Wright PC;Kalinowski J;Makarova KS;Bräsen C;Flemming HC;Wingender J;Siebers B
在代谢和细胞过程以及对极端环境的适应方面，海鲶是独一无二的。在过去的几年里，遗传系统和生物化学，遗传学和多组学研究的发展提供了一些古模式生物的生理学的深刻见解。酸热硫化叶菌是一种嗜热嗜酸泉古菌，最适生长温度为80°C，pH值为2至3。由于其独特的生理特性，允许在极端环境下生活，以及最近可用的遗传工具，这种极端微生物在生物技术应用中受到越来越多的关注。为了阐明耐受过程相关胁迫条件的潜力，我们研究了S。acidocaldarius转向工业相关有机溶剂1-丁醇。丁醇暴露后，S.在高达1.5%（体积/体积）的1-丁醇中，热酸菌得到增强并发生，而在高达1%（体积/体积）的1-丁醇中观察到嗜热酸菌的生长。共聚焦激光扫描显微镜显示，生物膜结构的变化，形成更密集和更高的塔状结构。同时，在1-丁醇暴露的生物膜中测定了具有增强的碳水化合物和蛋白质含量的细胞外聚合物的变化。使用扫描电子显微镜，观察到三种不同的细胞形态类型的1-丁醇。进行转录组和蛋白质组分析，比较在1-丁醇存在和不存在的情况下，嗜酸性细胞和生物膜细胞的反应。响应于1%（体积/体积）的1-丁醇，编码运动和细胞包膜结构，以及膜蛋白的基因的转录水平降低。细胞分裂和/或囊泡形成上调。此外，还观察到免疫和防御系统以及新陈代谢和一般应激反应的变化。我们的研究结果表明，极端的生活方式的S。酸热菌与对有机溶剂的高耐受性相一致。这项研究提供了什么可能是第一个洞察生物膜的形成和膜/细胞的压力所造成的有机溶剂在S。酸热菌。重要性海蛞蝓在代谢和细胞过程以及对极端环境的适应方面是独特的。在过去的几年里，遗传系统和生物化学，遗传学和多组学研究的发展提供了一些古模式生物的生理学的深刻见解。在这项研究中，我们使用S。嗜酸热菌，其适应于低pH和高温的两个极端，以研究其耐受性和稳健性以及其对有机溶剂的整体细胞响应，如1-丁醇。我们能够确定生物膜形成作为1-丁醇的主要细胞反应。此外，触发的细胞/膜应激导致培养物异质性的显著变化，伴随着中央细胞过程的变化，如细胞分裂和细胞防御系统，从而表明在群体水平上的保护的全球响应。
Archaea are unique in terms of metabolic and cellular processes, as well as the adaptation to extreme environments. In the past few years, the development of genetic systems and biochemical, genetic, and polyomics studies has provided deep insights into the physiology of some archaeal model organisms. Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80°C and pH 2 to 3. Due to its unique physiological properties, allowing life at environmental extremes, and the recent availability of genetic tools, this extremophile has received increasing interest for biotechnological applications. In order to elucidate the potential of tolerating process-related stress conditions, we investigated the response of S. acidocaldarius toward the industrially relevant organic solvent 1-butanol. In response to butanol exposure, biofilm formation of S. acidocaldarius was enhanced and occurred at up to 1.5% (vol/vol) 1-butanol, while planktonic growth was observed at up to 1% (vol/vol) 1-butanol. Confocal laser-scanning microscopy revealed that biofilm architecture changed with the formation of denser and higher tower-like structures. Concomitantly, changes in the extracellular polymeric substances with enhanced carbohydrate and protein content were determined in 1-butanol-exposed biofilms. Using scanning electron microscopy, three different cell morphotypes were observed in response to 1-butanol. Transcriptome and proteome analyses were performed comparing the response of planktonic and biofilm cells in the absence and presence of 1-butanol. In response to 1% (vol/vol) 1-butanol, transcript levels of genes encoding motility and cell envelope structures, as well as membrane proteins, were reduced. Cell division and/or vesicle formation were upregulated. Furthermore, changes in immune and defense systems, as well as metabolism and general stress responses, were observed. Our findings show that the extreme lifestyle of S. acidocaldarius coincided with a high tolerance to organic solvents. This study provides what may be the first insights into biofilm formation and membrane/cell stress caused by organic solvents in S. acidocaldarius. IMPORTANCE Archaea are unique in terms of metabolic and cellular processes, as well as the adaptation to extreme environments. In the past few years, the development of genetic systems and biochemical, genetic, and polyomics studies has provided deep insights into the physiology of some archaeal model organisms. In this study, we used S. acidocaldarius, which is adapted to the two extremes of low pH and high temperature, to study its tolerance and robustness as well as its global cellular response toward organic solvents, as exemplified by 1-butanol. We were able to identify biofilm formation as a primary cellular response to 1-butanol. Furthermore, the triggered cell/membrane stress led to significant changes in culture heterogeneity accompanied by changes in central cellular processes, such as cell division and cellular defense systems, thus suggesting a global response for the protection at the population level.