Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure

Benninghoff JC, Kuschmierz L, Zhou X, Albersmeier A, Pham TK, Busche T, Wright PC, Kalinowski J, Makarova KS, Brasen C, Flemming H-C, et al. (2021)
Applied and environmental microbiology.

Zeitschriftenaufsatz | E-Veröff. vor dem Druck | Englisch
 
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Autor*in
Benninghoff, Jens C; Kuschmierz, Laura; Zhou, Xiaoxiao; Albersmeier, AndreasUniBi; Pham, Trong Khoa; Busche, TobiasUniBi; Wright, Phillip C; Kalinowski, JörnUniBi; Makarova, Kira S; Brasen, Christopher; Flemming, Hans-Curt; Wingender, Jost
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Abstract / Bemerkung
Sulfolobus acidocaldarius is a thermoacidophilic crenarchaeon with optimal growth at 80 °C and pH 2 - 3. Due to its unique physiological properties allowing life at environmental extremes and recent availability of genetic tools, this extremophile receives increasing interest for biotechnological application. In order to elucidate the potential of tolerating process-related stress conditions, we investigated the response of S. acidocaldarius towards the industrially relevant organic solvent 1-butanol.In response to butanol exposure, biofilm formation of S. acidocaldarius was enhanced and occurred up to 1.5% (v/v) 1-butanol, while planktonic growth was only observed up to 1% (v/v) 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 absence and presence of 1-butanol. In response to 1% (v/v) 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 was upregulated. Furthermore, changes of immune and defence systems, as well as metabolism and general stress response were observed. Our findings show that the extreme lifestyle of S. acidocaldarius coincided with a high tolerance to organic solvents. This study provides first insights into biofilm formation and membrane/cell stress caused by organic solvents in S. acidocaldarius ImportanceArchaea 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 poly-omics studies have provided deep insights into the physiology of some archaeal model organisms. In this study, we used S. acidocaldarius adapted to two extremes, low pH and high temperature, to study its tolerance and robustness as well as its global cellular response towards organic solvents exemplified by 1-butanol. We were able to identify biofilm formation as 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 population level. Copyright © 2021 Benninghoff et al.
Erscheinungsjahr
2021
Zeitschriftentitel
Applied and environmental microbiology
eISSN
1098-5336
Page URI
https://pub.uni-bielefeld.de/record/2952997

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Benninghoff JC, Kuschmierz L, Zhou X, et al. Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure. Applied and environmental microbiology. 2021.
Benninghoff, J. C., Kuschmierz, L., Zhou, X., Albersmeier, A., Pham, T. K., Busche, T., Wright, P. C., et al. (2021). Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure. Applied and environmental microbiology. https://doi.org/10.1128/AEM.02988-20
Benninghoff, J. C., Kuschmierz, L., Zhou, X., Albersmeier, A., Pham, T. K., Busche, T., Wright, P. C., Kalinowski, J., Makarova, K. S., Brasen, C., et al. (2021). Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure. Applied and environmental microbiology.
Benninghoff, J.C., et al., 2021. Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure. Applied and environmental microbiology.
J.C. Benninghoff, et al., “Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure”, Applied and environmental microbiology, 2021.
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.-C., Wingender, J., Siebers, B.: Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure. Applied and environmental microbiology. (2021).
Benninghoff, Jens C, Kuschmierz, Laura, Zhou, Xiaoxiao, Albersmeier, Andreas, Pham, Trong Khoa, Busche, Tobias, Wright, Phillip C, Kalinowski, Jörn, Makarova, Kira S, Brasen, Christopher, Flemming, Hans-Curt, Wingender, Jost, and Siebers, Bettina. “Response of the thermoacidophilic Archaeon Sulfolobus acidocaldarius to solvent stress exemplified by 1-butanol exposure”. Applied and environmental microbiology (2021).

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