Benninghoff, Jens C.; Kuschmierz, Laura; Zhou, Xiaoxiao; Albersmeier, Andreas; Pham, Trong Khoa; Busche, Tobias; Wright, Phillip C.; Kalinowski, Jörn; Makarova, Kira S.; Bräsen, Christopher; Flemming, Hans-Curt; Wingender, Jost; Siebers, Bettina:
Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress
In: Applied and Environmental Microbiology, Vol. 87 (2021), No. 11
2021article/chapter in journalOA Hybrid
ChemistryFaculty of Chemistry » Biofilm CenterScientific institutes » Center of Medical Biotechnology (ZMB)
Related: 1 publication(s)
Title in English:
Exposure to 1-Butanol Exemplifies the Response of the Thermoacidophilic Archaeon Sulfolobus acidocaldarius to Solvent Stress
Author:
Benninghoff, Jens C.
;
Kuschmierz, Laura
;
Zhou, XiaoxiaoUDE
LSF ID
56249
Other
connected with university
;
Albersmeier, Andreas
;
Pham, Trong Khoa
;
Busche, Tobias
;
Wright, Phillip C.
;
Kalinowski, Jörn
;
Makarova, Kira S.
;
Bräsen, ChristopherUDE
LSF ID
52891
Other
connected with university
;
Flemming, Hans-CurtUDE
LSF ID
11401
ORCID
0000-0002-3670-9236ORCID iD
Other
connected with university
;
Wingender, JostUDE
LSF ID
11404
ORCID
0000-0003-3143-4760ORCID iD
Other
connected with university
;
Siebers, BettinaUDE
GND
142289736
LSF ID
49875
ORCID
0000-0002-9905-541XORCID iD
Other
connected with university
Year of publication:
2021
Open Access?:
OA Hybrid
Web of Science ID
PubMed ID
Scopus ID
Language of text:
English
Keyword, Topic:
1-butanol ; Archaea ; biofilm ; extracellular polymeric substances ; extremophiles ; organic solvent ; stress response ; Sulfolobus acidocaldarius

Abstract in English:

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. acidocaldariusIMPORTANCEArchaea 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.