Early Response of Sulfolobus acidocaldarius to Nutrient Limitation

Bischof LF, Haurat MF, Hoffmann L, Albersmeier A, Wolf J, Neu A, Pham TK, Albaum S, Jakobi T, Schouten S, Neumann-Schaal M, et al. (2019)
FRONTIERS IN MICROBIOLOGY 9: 3201.

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Abstract / Bemerkung
In natural environments microorganisms encounter extreme changes in temperature, pH, osmolarities and nutrient availability. The stress response of many bacterial species has been described in detail, however, knowledge in Archaea is limited. Here, we describe the cellular response triggered by nutrient limitation in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. We measured changes in gene transcription and protein abundance upon nutrient depletion up to 4 h after initiation of nutrient depletion. Transcript levels of 1118 of 2223 protein coding genes and abundance of approximately 500 proteins with functions in almost all cellular processes were affected by nutrient depletion. Our study reveals a significant rerouting of the metabolism with respect to degradation of internal as well as extracellular-bound organic carbon and degradation of proteins. Moreover, changes in membrane lipid composition were observed in order to access alternative sources of energy and to maintain pH homeostasis. At transcript level, the cellular response to nutrient depletion in S. acidocaldarius seems to be controlled by the general transcription factors TFB2 and TFE beta. In addition, ribosome biogenesis is reduced, while an increased protein degradation is accompanied with a loss of protein quality control. This study provides first insights into the early cellular response of Sulfolobus to organic carbon and organic nitrogen depletion.
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FRONTIERS IN MICROBIOLOGY
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9
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3201
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Bischof LF, Haurat MF, Hoffmann L, et al. Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. FRONTIERS IN MICROBIOLOGY. 2019;9: 3201.
Bischof, L. F., Haurat, M. F., Hoffmann, L., Albersmeier, A., Wolf, J., Neu, A., Pham, T. K., et al. (2019). Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. FRONTIERS IN MICROBIOLOGY, 9, 3201. doi:10.3389/fmicb.2018.03201
Bischof, L. F., Haurat, M. F., Hoffmann, L., Albersmeier, A., Wolf, J., Neu, A., Pham, T. K., Albaum, S., Jakobi, T., Schouten, S., et al. (2019). Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. FRONTIERS IN MICROBIOLOGY 9:3201.
Bischof, L.F., et al., 2019. Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. FRONTIERS IN MICROBIOLOGY, 9: 3201.
L.F. Bischof, et al., “Early Response of Sulfolobus acidocaldarius to Nutrient Limitation”, FRONTIERS IN MICROBIOLOGY, vol. 9, 2019, : 3201.
Bischof, L.F., Haurat, M.F., Hoffmann, L., Albersmeier, A., Wolf, J., Neu, A., Pham, T.K., Albaum, S., Jakobi, T., Schouten, S., Neumann-Schaal, M., Wright, P.C., Kalinowski, J., Siebers, B., Albers, S.-V.: Early Response of Sulfolobus acidocaldarius to Nutrient Limitation. FRONTIERS IN MICROBIOLOGY. 9, : 3201 (2019).
Bischof, Lisa F., Haurat, M. Florencia, Hoffmann, Lena, Albersmeier, Andreas, Wolf, Jacqueline, Neu, Astrid, Pham, Trong Khoa, Albaum, Stefan, Jakobi, Tobias, Schouten, Stefan, Neumann-Schaal, Meina, Wright, Phillip C., Kalinowski, Jörn, Siebers, Bettina, and Albers, Sonja-Verena. “Early Response of Sulfolobus acidocaldarius to Nutrient Limitation”. FRONTIERS IN MICROBIOLOGY 9 (2019): 3201.

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92 References

Daten bereitgestellt von Europe PubMed Central.

Involvement of a eukaryotic-like ubiquitin-related modifier in the proteasome pathway of the archaeon Sulfolobus acidocaldarius.
Anjum RS, Bray SM, Blackwood JK, Kilkenny ML, Coelho MA, Foster BM, Li S, Howard JA, Pellegrini L, Albers SV, Deery MJ, Robinson NP., Nat Commun 6(), 2015
PMID: 26348592
Life in acid: pH homeostasis in acidophiles.
Baker-Austin C, Dopson M., Trends Microbiol. 15(4), 2007
PMID: 17331729
The RpoS-mediated general stress response in Escherichia coli.
Battesti A, Majdalani N, Gottesman S., Annu. Rev. Microbiol. 65(), 2011
PMID: 21639793
Proteomic evaluation and validation of cathepsin D regulated proteins in macrophages exposed to Streptococcus pneumoniae.
Bewley MA, Pham TK, Marriott HM, Noirel J, Chu HP, Ow SY, Ryazanov AG, Read RC, Whyte MK, Chain B, Wright PC, Dockrell DH., Mol. Cell Proteomics 10(6), 2011
PMID: 21474794
Archaeal TFEα/β is a hybrid of TFIIE and the RNA polymerase III subcomplex hRPC62/39.
Blombach F, Salvadori E, Fouqueau T, Yan J, Reimann J, Sheppard C, Smollett KL, Albers SV, Kay CW, Thalassinos K, Werner F., Elife 4(), 2015
PMID: 26067235
Carbohydrate metabolism in Archaea: current insights into unusual enzymes and pathways and their regulation.
Brasen C, Esser D, Rauch B, Siebers B., Microbiol. Mol. Biol. Rev. 78(1), 2014
PMID: 24600042
The Sulfolobus solfataricus Lrp-like protein LysM regulates lysine biosynthesis in response to lysine availability.
Brinkman AB, Bell SD, Lebbink RJ, de Vos WM, van der Oost J., J. Biol. Chem. 277(33), 2002
PMID: 12042311
Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature.
Brock TD, Brock KM, Belly RT, Weiss RL., Arch Mikrobiol 84(1), 1972
PMID: 4559703
Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes.
Buetti-Dinh A, Dethlefsen O, Friedman R, Dopson M., Microbiology (Reading, Engl.) 162(8), 2016
PMID: 27230583
Stringent control in the archaeal genus Sulfolobus.
Cellini A, Scoarughi GL, Poggiali P, Santino I, Sessa R, Donini P, Cimmino C., Res. Microbiol. 155(2), 2004
PMID: 14990261
Stringency and relaxation among the halobacteria.
Cimmino C, Scoarughi GL, Donini P., J. Bacteriol. 175(20), 1993
PMID: 7691798
Unraveling the function of paralogs of the aldehyde dehydrogenase super family from Sulfolobus solfataricus.
Esser D, Kouril T, Talfournier F, Polkowska J, Schrader T, Brasen C, Siebers B., Extremophiles 17(2), 2013
PMID: 23296511
Identification and functional verification of archaeal-type phosphoenolpyruvate carboxylase, a missing link in archaeal central carbohydrate metabolism.
Ettema TJ, Makarova KS, Jellema GL, Gierman HJ, Koonin EV, Huynen MA, de Vos WM, van der Oost J., J. Bacteriol. 186(22), 2004
PMID: 15516590
General transcription factor specified global gene regulation in archaea.
Facciotti MT, Reiss DJ, Pan M, Kaur A, Vuthoori M, Bonneau R, Shannon P, Srivastava A, Donohoe SM, Hood LE, Baliga NS., Proc. Natl. Acad. Sci. U.S.A. 104(11), 2007
PMID: 17360575
A transcriptional factor B paralog functions as an activator to DNA damage-responsive expression in archaea.
Feng X, Sun M, Han W, Liang YX, She Q., Nucleic Acids Res. 46(14), 2018
PMID: 29618058
Molecular modeling of archaebacterial bipolar tetraether lipid membranes.
Gabriel JL, Chong PL., Chem. Phys. Lipids 105(2), 2000
PMID: 10823467
The archaeal SoxABCD complex is a proton pump in Sulfolobus acidocaldarius.
Gleissner M, Kaiser U, Antonopoulos E, Schafer G., J. Biol. Chem. 272(13), 1997
PMID: 9079667
ArnS, a kinase involved in starvation-induced archaellum expression.
Haurat MF, Figueiredo AS, Hoffmann L, Li L, Herr K, J Wilson A, Beeby M, Schaber J, Albers SV., Mol. Microbiol. 103(1), 2016
PMID: 27731916
ReadXplorer--visualization and analysis of mapped sequences.
Hilker R, Stadermann KB, Doppmeier D, Kalinowski J, Stoye J, Straube J, Winnebald J, Goesmann A., Bioinformatics 30(16), 2014
PMID: 24790157
Expanding the archaellum regulatory network - the eukaryotic protein kinases ArnC and ArnD influence motility of Sulfolobus acidocaldarius.
Hoffmann L, Schummer A, Reimann J, Haurat MF, Wilson AJ, Beeby M, Warscheid B, Albers SV., Microbiologyopen 6(1), 2016
PMID: 27771939
The effect of improved chromatography on GDGT-based palaeoproxies.
Hopmans E., Schouten S., Sinninghe J.., 2016
Transcriptional profiling of Caulobacter crescentus during growth on complex and minimal media.
Hottes AK, Meewan M, Yang D, Arana N, Romero P, McAdams HH, Stephens C., J. Bacteriol. 186(5), 2004
PMID: 14973021
Triggering the stringent response: signals responsible for activating (p)ppGpp synthesis in bacteria.
Irving SE, Corrigan RM., Microbiology (Reading, Engl.) 164(3), 2018
PMID: 29493495
N-linked glycosylation in Archaea: a structural, functional, and genetic analysis.
Jarrell KF, Ding Y, Meyer BH, Albers SV, Kaminski L, Eichler J., Microbiol. Mol. Biol. Rev. 78(2), 2014
PMID: 24847024
Proteome profiling of heat, oxidative, and salt stress responses in Thermococcus kodakarensis KOD1.
Jia B, Liu J, Van Duyet L, Sun Y, Xuan YH, Cheong GW., Front Microbiol 6(), 2015
PMID: 26150806
Transcription in archaea: similarity to that in eucarya.
Langer D, Hain J, Thuriaux P, Zillig W., Proc. Natl. Acad. Sci. U.S.A. 92(13), 1995
PMID: 7597027
Fast gapped-read alignment with Bowtie 2.
Langmead B, Salzberg SL., Nat. Methods 9(4), 2012
PMID: 22388286
Molecular analysis of the crenarchaeal flagellum.
Lassak K, Neiner T, Ghosh A, Klingl A, Wirth R, Albers SV., Mol. Microbiol. 83(1), 2011
PMID: 22081969
The one-component system ArnR: a membrane-bound activator of the crenarchaeal archaellum.
Lassak K, Peeters E, Wrobel S, Albers SV., Mol. Microbiol. 88(1), 2013
PMID: 23461567
Wing phosphorylation is a major functional determinant of the Lrs14-type biofilm and motility regulator AbfR1 in Sulfolobus acidocaldarius.
Li L, Banerjee A, Bischof LF, Maklad HR, Hoffmann L, Henche AL, Veliz F, Bildl W, Schulte U, Orell A, Essen LO, Peeters E, Albers SV., Mol. Microbiol. 105(5), 2017
PMID: 28628237
BarR, an Lrp-type transcription factor in Sulfolobus acidocaldarius, regulates an aminotransferase gene in a β-alanine responsive manner.
Liu H, Orell A, Maes D, van Wolferen M, Lindas AC, Bernander R, Albers SV, Charlier D, Peeters E., Mol. Microbiol. 92(3), 2014
PMID: 24646198
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
Love MI, Huber W, Anders S., Genome Biol. 15(12), 2014
PMID: 25516281
A second terminal oxidase in Sulfolobus acidocaldarius.
Lubben M, Arnaud S, Castresana J, Warne A, Albracht SP, Saraste M., Eur. J. Biochem. 224(1), 1994
PMID: 8076636
The purified SoxABCD quinol oxidase complex of Sulfolobus acidocaldarius contains a novel haem.
Lubben M, Warne A, Albracht SP, Saraste M., Mol. Microbiol. 13(2), 1994
PMID: 7984110
Genome-wide transcription map of an archaeal cell cycle.
Lundgren M, Bernander R., Proc. Natl. Acad. Sci. U.S.A. 104(8), 2007
PMID: 17307872
Something old, something new, something borrowed; how the thermoacidophilic archaeon Sulfolobus solfataricus responds to oxidative stress.
Maaty WS, Wiedenheft B, Tarlykov P, Schaff N, Heinemann J, Robison-Cox J, Valenzuela J, Dougherty A, Blum P, Lawrence CM, Douglas T, Young MJ, Bothner B., PLoS ONE 4(9), 2009
PMID: 19759909
ppGpp: a global regulator in Escherichia coli.
Magnusson LU, Farewell A, Nystrom T., Trends Microbiol. 13(5), 2005
PMID: 15866041
Organic solutes in hyperthermophilic archaea.
Martins LO, Huber R, Huber H, Stetter KO, Da Costa MS, Santos H., Appl. Environ. Microbiol. 63(3), 1997
PMID: 16535556
Cloning and sequencing of a cluster of genes encoding novel enzymes of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius.
Maruta K, Mitsuzumi H, Nakada T, Kubota M, Chaen H, Fukuda S, Sugimoto T, Kurimoto M., Biochim. Biophys. Acta 1291(3), 1996
PMID: 8980629
Sulfoquinovose synthase - an important enzyme in the N-glycosylation pathway of Sulfolobus acidocaldarius.
Meyer BH, Zolghadr B, Peyfoon E, Pabst M, Panico M, Morris HR, Haslam SM, Messner P, Schaffer C, Dell A, Albers SV., Mol. Microbiol. 82(5), 2011
PMID: 22059775
Chemiosmotic H + cycling across the plasma membrane of the thermoacidophilic archaebacterium Sulfolobus acidocaldarius.
Moll R., Schäfer G.., 1988
Characterization of a trehalose-degrading enzyme from the hyperthermophilic archaeon Sulfolobus acidocaldarius.
Moon JH, Lee W, Park J, Choi KH, Cha J., J. Biosci. Bioeng. 122(1), 2016
PMID: 26811220
Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea.
Orell A, Peeters E, Vassen V, Jachlewski S, Schalles S, Siebers B, Albers SV., ISME J 7(10), 2013
PMID: 23657363
Adaptive response of the archaeon Sulfolobus acidocaldarius BC65 to phosphate starvation.
Osorio G, Jerez CA., Microbiology (Reading, Engl.) 142 ( Pt 6)(), 1996
PMID: 8704993
Lysine and arginine biosyntheses mediated by a common carrier protein in Sulfolobus.
Ouchi T, Tomita T, Horie A, Yoshida A, Takahashi K, Nishida H, Lassak K, Taka H, Mineki R, Fujimura T, Kosono S, Nishiyama C, Masui R, Kuramitsu S, Albers SV, Kuzuyama T, Nishiyama M., Nat. Chem. Biol. 9(4), 2013
PMID: 23434852
An expanding family of archaeal transcriptional activators.
Ouhammouch M, Geiduschek EP., Proc. Natl. Acad. Sci. U.S.A. 102(43), 2005
PMID: 16230629
The Lrp family of transcription regulators in archaea.
Peeters E, Charlier D., Archaea 2010(), 2010
PMID: 21151646
A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia.
Pham TK, Roy S, Noirel J, Douglas I, Wright PC, Stafford GP., Proteomics 10(17), 2010
PMID: 20806225
Regulation of archaella expression by the FHA and von Willebrand domain-containing proteins ArnA and ArnB in Sulfolobus acidocaldarius.
Reimann J, Lassak K, Khadouma S, Ettema TJ, Yang N, Driessen AJ, Klingl A, Albers SV., Mol. Microbiol. 86(1), 2012
PMID: 22845497
Biochemical relationship of phosphoenolpyruvate carboxylases (PEPCs) from thermophilic archaea.
Sako Y., Takai K., Nishizaka T., Ishida Y.., 1997
Trehalose production: exploiting novel approaches.
Schiraldi C, Di Lernia I, De Rosa M., Trends Biotechnol. 20(10), 2002
PMID: 12220904
Effect of UV irradiation on Sulfolobus acidocaldarius and involvement of the general transcription factor TFB3 in the early UV response.
Schult F, Le TN, Albersmeier A, Rauch B, Blumenkamp P, van der Does C, Goesmann A, Kalinowski J, Albers SV, Siebers B., Nucleic Acids Res. 46(14), 2018
PMID: 29982548
The archaellum: a rotating type IV pilus.
Shahapure R, Driessen RP, Haurat MF, Albers SV, Dame RT., Mol. Microbiol. 91(4), 2014
PMID: 24330313
Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure.
Siliakus MF, van der Oost J, Kengen SWM., Extremophiles 21(4), 2017
PMID: 28508135
Effect of O2 concentrations on Sulfolobus solfataricus P2.
Simon G, Walther J, Zabeti N, Combet-Blanc Y, Auria R, van der Oost J, Casalot L., FEMS Microbiol. Lett. 299(2), 2009
PMID: 19735462
Cytoplasmic pH measurement and homeostasis in bacteria and archaea.
Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA., Adv. Microb. Physiol. 55(), 2009
PMID: 19573695
Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus.
Stark H, Wolf J, Albersmeier A, Pham TK, Hofmann JD, Siebers B, Kalinowski J, Wright PC, Neumann-Schaal M, Schomburg D., FEBS J. 284(13), 2017
PMID: 28497654
Variation in molecular species of core lipids from the order thermoplasmales strains depends on the growth temperature.
Uda I., Sugai A., Itoh Y., Itoh T.., 2004
A novel archaeal transcriptional regulator of heat shock response.
Vierke G, Engelmann A, Hebbeln C, Thomm M., J. Biol. Chem. 278(1), 2002
PMID: 12381724
2016 update of the PRIDE database and its related tools.
Vizcaino JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, Xu QW, Wang R, Hermjakob H., Nucleic Acids Res. 44(D1), 2015
PMID: 26527722
Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius.
Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer BH, Reimann J, Albers SV., Front Microbiol 3(), 2012
PMID: 22707949
A systems biology approach reveals major metabolic changes in the thermoacidophilic archaeon Sulfolobus solfataricus in response to the carbon source L-fucose versus D-glucose.
Wolf J, Stark H, Fafenrot K, Albersmeier A, Pham TK, Muller KB, Meyer BH, Hoffmann L, Shen L, Albaum SP, Kouril T, Schmidt-Hohagen K, Neumann-Schaal M, Brasen C, Kalinowski J, Wright PC, Albers SV, Schomburg D, Siebers B., Mol. Microbiol. 102(5), 2016
PMID: 27611014
Ring index: a new strategy to evaluate the integrity of TEX86paleothermometry.
Zhang Y., Pagani M., Wang Z.., 2016

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