Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress
Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80 degrees 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 b...
| Main Authors: | , , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Journal Article |
| Language: | English |
| Published: |
2021
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| Subjects: | |
| Online Access: | https://hdl.handle.net/10356/153763 |
| _version_ | 1811688909581582336 |
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| author | Benninghoff, Jens C. Kuschmierz, Laura Zhou, Xiaoxiao Albersmeier, Andreas Pham, Trong Khoa Busche, Tobias Wright, Phillip C. Kalinowski, Jorn Makarova, Kira S. Brasen, Christopher Flemming, Hans-Curt Wingender, Jost Siebers, Bettina |
| author2 | Singapore Centre for Environmental Life Sciences and Engineering |
| author_facet | Singapore Centre for Environmental Life Sciences and Engineering Benninghoff, Jens C. Kuschmierz, Laura Zhou, Xiaoxiao Albersmeier, Andreas Pham, Trong Khoa Busche, Tobias Wright, Phillip C. Kalinowski, Jorn Makarova, Kira S. Brasen, Christopher Flemming, Hans-Curt Wingender, Jost Siebers, Bettina |
| author_sort | Benninghoff, Jens C. |
| collection | NTU |
| description | Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80 degrees 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. |
| first_indexed | 2024-10-01T05:39:42Z |
| format | Journal Article |
| id | ntu-10356/153763 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T05:39:42Z |
| publishDate | 2021 |
| record_format | dspace |
| spelling | ntu-10356/1537632021-12-18T20:12:30Z Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress Benninghoff, Jens C. Kuschmierz, Laura Zhou, Xiaoxiao Albersmeier, Andreas Pham, Trong Khoa Busche, Tobias Wright, Phillip C. Kalinowski, Jorn Makarova, Kira S. Brasen, Christopher Flemming, Hans-Curt Wingender, Jost Siebers, Bettina Singapore Centre for Environmental Life Sciences and Engineering Engineering::Environmental engineering Archaea Extremophiles Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80 degrees 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. Published version .C.B. acknowledges funding by the Mercator foundation for support with a Mercur startup grant (Pr-2011-0058) and by the German Federal Ministry of Education and Research (BMBF) grant SulfoSYSBIOTECH, 0316188A within the e:Bio funding initiative. A.A. was supported by grant 0316188D within SulfoSYSBIOTECH. L.K. acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG, SI 642/13-1). X.Z. acknowledges funding by the VW Stiftung in the “Life?” initiative (96725). K.S.M. is supported by the Intramural Research Program of the National Institutes of Health of the USA (National Library of Medicine). T.K.P. and P.C.W. acknowledge the BBSRC funding BB/M018172/1 and BB/M018288/1. 2021-12-16T06:34:28Z 2021-12-16T06:34:28Z 2021 Journal Article Benninghoff, J. C., Kuschmierz, L., Zhou, X., Albersmeier, A., Pham, T. K., Busche, T., Wright, P. C., Kalinowski, J., Makarova, K. S., Brasen, C., Flemming, H., Wingender, J. & Siebers, B. (2021). Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress. Applied and Environmental Microbiology, 87(11), e02988-20-. https://dx.doi.org/10.1128/AEM.02988-20 0099-2240 https://hdl.handle.net/10356/153763 10.1128/AEM.02988-20 11 87 e02988-20 en Applied and Environmental Microbiology © 2021 Benninghoff et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. application/pdf |
| spellingShingle | Engineering::Environmental engineering Archaea Extremophiles Benninghoff, Jens C. Kuschmierz, Laura Zhou, Xiaoxiao Albersmeier, Andreas Pham, Trong Khoa Busche, Tobias Wright, Phillip C. Kalinowski, Jorn Makarova, Kira S. Brasen, Christopher Flemming, Hans-Curt Wingender, Jost Siebers, Bettina Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title | Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title_full | Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title_fullStr | Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title_full_unstemmed | Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title_short | Exposure to 1-butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| title_sort | exposure to 1 butanol exemplifies the response of the thermoacidophilic archaeon sulfolobus acidocaldarius to solvent stress |
| topic | Engineering::Environmental engineering Archaea Extremophiles |
| url | https://hdl.handle.net/10356/153763 |
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