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 (2017)
FEBS JOURNAL 284(13): 2078-2095.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Stark, Helge; Wolf, Jacqueline; Albersmeier, AndreasUniBi; Pham, Trong K.; Hofmann, Julia D.; Siebers, Bettina; Kalinowski, JörnUniBi; Wright, Phillip C.; Neumann-Schaal, Meina; Schomburg, Dietmar
Abstract / Bemerkung
The thermoacidophilic Crenarchaeon Sulfolobus solfataricus is a model organism for archaeal adaptation to extreme environments and renowned for its ability to degrade a broad variety of substrates. It has been well characterised concerning the utilisation of numerous carbohydrates as carbon source. However, its amino acid metabolism, especially the degradation of single amino acids, is not as well understood. In this work, we performed metabolic modelling as well as metabolome, transcriptome and proteome analysis on cells grown on caseinhydrolysate as carbon source in order to draw a comprehensive picture of amino acid metabolism in S. solfataricus P2. We found that 10 out of 16 detectable amino acids are imported from the growth medium. Overall, uptake of glutamate, methionine, leucine, phenylalanine and isoleucine was the highest of all observed amino acids. Our simulations predict an incomplete degradation of leucine and tyrosine to organic acids, and in accordance with this, we detected the export of branched-chain and aromatic organic acids as well as amino acids, ammonium and trehalose into the culture supernatants. The branched-chain amino acids as well as phenylalanine and tyrosine are degraded to organic acids via oxidative Stickland reactions. Such reactions are known for prokaryotes capable of anaerobic growth, but so far have never been observed in an obligate aerobe. Also, 3-methyl-2-butenoate and 2-methyl-2-butenoate are for the first time found as products of modified Stickland reactions for the degradation of branched-chain amino acids. This work presents the first detailed description of branched-chain and aromatic amino acid catabolism in S. solfataricus.
amino acid degradation; biological model; Stickland reactions; Sulfolobus; systems biology
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Stark H, Wolf J, Albersmeier A, et al. Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus. FEBS JOURNAL. 2017;284(13):2078-2095.
Stark, H., Wolf, J., Albersmeier, A., Pham, T. K., Hofmann, J. D., Siebers, B., Kalinowski, J., et al. (2017). Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus. FEBS JOURNAL, 284(13), 2078-2095. doi:10.1111/febs.14105
Stark, H., Wolf, J., Albersmeier, A., Pham, T. K., Hofmann, J. D., Siebers, B., Kalinowski, J., Wright, P. C., Neumann-Schaal, M., and Schomburg, D. (2017). Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus. FEBS JOURNAL 284, 2078-2095.
Stark, H., et al., 2017. Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus. FEBS JOURNAL, 284(13), p 2078-2095.
H. Stark, et al., “Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus”, FEBS JOURNAL, vol. 284, 2017, pp. 2078-2095.
Stark, H., Wolf, J., Albersmeier, A., Pham, T.K., Hofmann, J.D., Siebers, B., Kalinowski, J., Wright, P.C., Neumann-Schaal, M., Schomburg, D.: Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus. FEBS JOURNAL. 284, 2078-2095 (2017).
Stark, Helge, Wolf, Jacqueline, Albersmeier, Andreas, Pham, Trong K., Hofmann, Julia D., Siebers, Bettina, Kalinowski, Jörn, Wright, Phillip C., Neumann-Schaal, Meina, and Schomburg, Dietmar. “Oxidative Stickland reactions in an obligate aerobic organism - amino acid catabolism in the Crenarchaeon Sulfolobus solfataricus”. FEBS JOURNAL 284.13 (2017): 2078-2095.

4 Zitationen in Europe PMC

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Kinetic modeling of Stickland reactions-coupled methanogenesis for a methanogenic culture.
Sangavai C, Bharathi M, Ganesh SP, Chellapandi P., AMB Express 9(1), 2019
PMID: 31183623
Early Response of Sulfolobus acidocaldarius to Nutrient Limitation.
Bischof LF, Haurat MF, Hoffmann L, Albersmeier A, Wolf J, Neu A, Pham TK, Albaum SP, Jakobi T, Schouten S, Neumann-Schaal M, Wright PC, Kalinowski J, Siebers B, Albers SV., Front Microbiol 9(), 2018
PMID: 30687244
Sulfolobus - A Potential Key Organism in Future Biotechnology.
Quehenberger J, Shen L, Albers SV, Siebers B, Spadiut O., Front Microbiol 8(), 2017
PMID: 29312184

63 References

Daten bereitgestellt von Europe PubMed Central.

Extremely thermophilic acidophilic bacteria convergent with Sulfolobus acidocaldarius.
de Rosa M, Gambacorta A, Bu'lock JD., J. Gen. Microbiol. 86(1), 1975
PMID: 234504
The Sulfolobus-”Caldariella” group: taxonomy on the basis of the structure of DNA-dependent RNA polymerases
Zillig, Arch Microbiol 125(), 1980
Adaptation of Sulfolobus solfataricus on minimal media
Nicolaus, Biotechnol Lett 13(), 1991
The thermophilic archaeon Sulfolobus solfataricus is able to grow on phenol.
Izzo V, Notomista E, Picardi A, Pennacchio F, Di Donato A., Res. Microbiol. 156(5-6), 2005
PMID: 15921893
Glucose metabolism in the extreme thermoacidophilic archaebacterium Sulfolobus solfataricus.
De Rosa M, Gambacorta A, Nicolaus B, Giardina P, Poerio E, Buonocore V., Biochem. J. 224(2), 1984
PMID: 6440533
Identification of the missing links in prokaryotic pentose oxidation pathways: evidence for enzyme recruitment.
Brouns SJ, Walther J, Snijders AP, van de Werken HJ, Willemen HL, Worm P, de Vos MG, Andersson A, Lundgren M, Mazon HF, van den Heuvel RH, Nilsson P, Salmon L, de Vos WM, Wright PC, Bernander R, van der Oost J., J. Biol. Chem. 281(37), 2006
PMID: 16849334
Metabolism of pentose sugars in the hyperthermophilic archaea Sulfolobus solfataricus and Sulfolobus acidocaldarius.
Nunn CE, Johnsen U, Schonheit P, Fuhrer T, Sauer U, Hough DW, Danson MJ., J. Biol. Chem. 285(44), 2010
PMID: 20736170
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
2-Propanol degradation by Sulfolobus solfataricus.
Radianingtyas H, Wright PC., Biotechnol. Lett. 25(7), 2003
PMID: 12882148
Proteome analysis of Sulfolobus solfataricus P2 propanol metabolism.
Chong PK, Burja AM, Radianingtyas H, Fazeli A, Wright PC., J. Proteome Res. 6(4), 2007
PMID: 17315908
Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature
Brock, Arch Für Mikrobiol 84(), 1972
The complete genome of the crenarchaeon Sulfolobus solfataricus P2.
She Q, Singh RK, Confalonieri F, Zivanovic Y, Allard G, Awayez MJ, Chan-Weiher CC, Clausen IG, Curtis BA, De Moors A, Erauso G, Fletcher C, Gordon PM, Heikamp-de Jong I, Jeffries AC, Kozera CJ, Medina N, Peng X, Thi-Ngoc HP, Redder P, Schenk ME, Theriault C, Tolstrup N, Charlebois RL, Doolittle WF, Duguet M, Gaasterland T, Garrett RA, Ragan MA, Sensen CW, Van der Oost J., Proc. Natl. Acad. Sci. U.S.A. 98(14), 2001
PMID: 11427726
The glutamic acid-pyrrolidonecarboxylic acid system
Wilson, J Biol Chem 119(), 1937
Amino acid degradation by anaerobic bacteria.
Barker HA., Annu. Rev. Biochem. 50(), 1981
PMID: 6791576
The Stickland reaction.
NISMAN B., Bacteriol Rev 18(1), 1954
PMID: 13140081
The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus Ferrooxidans
Alexander, Microbiology 133(), 1987
Life in acid: pH homeostasis in acidophiles.
Baker-Austin C, Dopson M., Trends Microbiol. 15(4), 2007
PMID: 17331729
Another extreme genome: how to live at pH 0.
Ciaramella M, Napoli A, Rossi M., Trends Microbiol. 13(2), 2005
PMID: 15680761
Growth inhibition of Acidiphilium species by organic acids contained in yeast extract
Kishimoto, J Ferment Bioeng 70(), 1990
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
Energetics of bacterial growth: balance of anabolic and catabolic reactions.
Russell JB, Cook GM., Microbiol. Rev. 59(1), 1995
PMID: 7708012
Biochemical evidence supporting the presence of the classical mevalonate pathway in the thermoacidophilic archaeon Sulfolobus solfataricus.
Nishimura H, Azami Y, Miyagawa M, Hashimoto C, Yoshimura T, Hemmi H., J. Biochem. 153(5), 2013
PMID: 23378249
Dehydration of (R)-2-hydroxyacyl-CoA to enoyl-CoA in the fermentation of alpha-amino acids by anaerobic bacteria.
Kim J, Hetzel M, Boiangiu CD, Buckel W., FEMS Microbiol. Rev. 28(4), 2004
PMID: 15374661
Crystal structures of archaeal 2-oxoacid:ferredoxin oxidoreductases from Sulfolobus tokodaii.
Yan Z, Maruyama A, Arakawa T, Fushinobu S, Wakagi T., Sci Rep 6(), 2016
PMID: 27619895
2-keto acid oxidoreductases from Pyrococcus furiosus and Thermococcus litoralis.
Schut GJ, Menon AL, Adams MW., Meth. Enzymol. 331(), 2001
PMID: 11265457

Luengo, 2007
Bacterial phenylalanine and phenylacetate catabolic pathway revealed.
Teufel R, Mascaraque V, Ismail W, Voss M, Perera J, Eisenreich W, Haehnel W, Fuchs G., Proc. Natl. Acad. Sci. U.S.A. 107(32), 2010
PMID: 20660314
BRENDA in 2015: exciting developments in its 25th year of existence.
Chang A, Schomburg I, Placzek S, Jeske L, Ulbrich M, Xiao M, Sensen CW, Schomburg D., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25378310
Pyruvate metabolism of the hyperthermophilic archaebacterium Pyrococcus furiosus
Schäfer, Arch Microbiol 155(), 1991
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
Bioenergetics of the Archaea.
Schafer G, Engelhard M, Muller V., Microbiol. Mol. Biol. Rev. 63(3), 1999
PMID: 10477309
The SEEK: a platform for sharing data and models in systems biology.
Wolstencroft K, Owen S, du Preez F, Krebs O, Mueller W, Goble C, Snoep JL., Meth. Enzymol. 500(), 2011
PMID: 21943917
Glutamate dehydrogenase from the thermoacidophilic archaebacterium Sulfolobus solfataricus.
Consalvi V, Chiaraluce R, Politi L, Gambacorta A, De Rosa M, Scandurra R., Eur. J. Biochem. 196(2), 1991
PMID: 1901040
Purification and characterization of aspartate aminotransferase from the thermoacidophilic archaebacterium Sulfolobus solfataricus.
Marino G, Nitti G, Arnone MI, Sannia G, Gambacorta A, De Rosa M., J. Biol. Chem. 263(25), 1988
PMID: 3137225
Biosynthesis of archaeal membrane ether lipids
Jain, Microb Physiol Metab 5(), 2014
Unusual enzymes involved in five pathways of glutamate fermentation.
Buckel W., Appl. Microbiol. Biotechnol. 57(3), 2001
PMID: 11759672
Time-resolved amino acid uptake of Clostridium difficile 630Δerm and concomitant fermentation product and toxin formation.
Neumann-Schaal M, Hofmann JD, Will SE, Schomburg D., BMC Microbiol. 15(), 2015
PMID: 26680234
"Hot standards" for the thermoacidophilic archaeon Sulfolobus solfataricus.
Zaparty M, Esser D, Gertig S, Haferkamp P, Kouril T, Manica A, Pham TK, Reimann J, Schreiber K, Sierocinski P, Teichmann D, van Wolferen M, von Jan M, Wieloch P, Albers SV, Driessen AJ, Klenk HP, Schleper C, Schomburg D, van der Oost J, Wright PC, Siebers B., Extremophiles 14(1), 2009
PMID: 19802714
Rapid Analysis of Cocaine in Saliva by Surface-Enhanced Raman Spectroscopy.
Dana K, Shende C, Huang H, Farquharson S., J Anal Bioanal Tech 6(6), 2015
PMID: 26819811
Native plasmids restrict growth of Phaeobacter inhibens DSM 17395: Energetic costs of plasmids assessed by quantitative physiological analyses.
Trautwein K, Will SE, Hulsch R, Maschmann U, Wiegmann K, Hensler M, Michael V, Ruppersberg H, Wunsch D, Feenders C, Neumann-Schaal M, Kaltenhauser S, Ulbrich M, Schmidt-Hohagen K, Blasius B, Petersen J, Schomburg D, Rabus R., Environ. Microbiol. 18(12), 2016
PMID: 27233797
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
Differential expression analysis for sequence count data.
Anders S, Huber W., Genome Biol. 11(10), 2010
PMID: 20979621


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