Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius
Abstract
Abstract Alicyclobacillus acidocaldarius is a thermoacidophilic bacterium capable of growth on sugars from plant biomass. Carbon catabolite repression (CCR) allows bacteria to focus cellular resources on a sugar that provides efficient growth, but also allows sequential, rather than simultaneous use when more than one sugar is present. The A. acidocaldarius genome encodes all components of CCR, but transporters encoded are multifacilitator superfamily and ATP-binding cassette-type transporters, uncommon for CCR. Therefore, global transcriptome analysis of A. acidocaldarius grown on xylose or fructose was performed in chemostats, followed by attempted induction of CCR with glucose or arabinose. Alicyclobacillus acidocaldarius grew while simultaneously metabolizing xylose and glucose, xylose and arabinose, and fructose and glucose, indicating that CCR did not control carbon metabolism. Microarrays showed down-regulation of genes during growth on one sugar compared to two, and occurred primarily in genes encoding: (1) regulators; (2) enzymes for cell wall synthesis; and (3) sugar transporters.
- Authors:
-
- grid.417824.c 0000 0001 0020 7392 Idaho National Laboratory Biological Systems Department Idaho Falls ID USA, 0000 0001 2169 6535 grid.257296.d Department of Biological Sciences Idaho State University Pocatello ID USA, grid.451303.0 0000 0001 2218 3491 Pacific Northwest National Laboratory Energy and Environment Directorate Richland WA USA
- grid.417824.c 0000 0001 0020 7392 Idaho National Laboratory Biological Systems Department Idaho Falls ID USA, Aspenglow Associates, LLC P. O. Box 12692 83002 Jackson WY USA
- 0000 0001 0704 1727 grid.263790.9 Department of Chemistry and Applied Biological Sciences South Dakota School of Mines and Technology Rapid City SD USA
- 0000 0001 2169 6535 grid.257296.d Department of Biological Sciences Idaho State University Pocatello ID USA
- Publication Date:
- Research Org.:
- Idaho National Lab. (INL), Idaho Falls, ID (United States)
- Sponsoring Org.:
- USDOE Office of Nuclear Energy (NE); INL Laboratory Directed Research and Development (LDRD) Program
- OSTI Identifier:
- 1773516
- Alternate Identifier(s):
- OSTI ID: 1375243
- Report Number(s):
- INL/JOU-16-39289
Journal ID: ISSN 1367-5435
- Grant/Contract Number:
- Laboratory Directed Research and Development; AC07-05ID14517
- Resource Type:
- Published Article
- Journal Name:
- Journal of Industrial Microbiology and Biotechnology
- Additional Journal Information:
- Journal Name: Journal of Industrial Microbiology and Biotechnology Journal Volume: 44 Journal Issue: 10; Journal ID: ISSN 1367-5435
- Publisher:
- Oxford University Press
- Country of Publication:
- Germany
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; alicyclobacillus acidocaldarius; lignocellulose; microarray; thermoacidophile
Citation Formats
Lee, Brady D., Apel, William A., DeVeaux, Linda C., and Sheridan, Peter P. Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius. Germany: N. p., 2017.
Web. doi:10.1007/s10295-017-1968-2.
Lee, Brady D., Apel, William A., DeVeaux, Linda C., & Sheridan, Peter P. Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius. Germany. https://doi.org/10.1007/s10295-017-1968-2
Lee, Brady D., Apel, William A., DeVeaux, Linda C., and Sheridan, Peter P. Sun .
"Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius". Germany. https://doi.org/10.1007/s10295-017-1968-2.
@article{osti_1773516,
title = {Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius},
author = {Lee, Brady D. and Apel, William A. and DeVeaux, Linda C. and Sheridan, Peter P.},
abstractNote = {Abstract Alicyclobacillus acidocaldarius is a thermoacidophilic bacterium capable of growth on sugars from plant biomass. Carbon catabolite repression (CCR) allows bacteria to focus cellular resources on a sugar that provides efficient growth, but also allows sequential, rather than simultaneous use when more than one sugar is present. The A. acidocaldarius genome encodes all components of CCR, but transporters encoded are multifacilitator superfamily and ATP-binding cassette-type transporters, uncommon for CCR. Therefore, global transcriptome analysis of A. acidocaldarius grown on xylose or fructose was performed in chemostats, followed by attempted induction of CCR with glucose or arabinose. Alicyclobacillus acidocaldarius grew while simultaneously metabolizing xylose and glucose, xylose and arabinose, and fructose and glucose, indicating that CCR did not control carbon metabolism. Microarrays showed down-regulation of genes during growth on one sugar compared to two, and occurred primarily in genes encoding: (1) regulators; (2) enzymes for cell wall synthesis; and (3) sugar transporters.},
doi = {10.1007/s10295-017-1968-2},
journal = {Journal of Industrial Microbiology and Biotechnology},
number = 10,
volume = 44,
place = {Germany},
year = {Sun Oct 01 00:00:00 EDT 2017},
month = {Sun Oct 01 00:00:00 EDT 2017}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1007/s10295-017-1968-2
https://doi.org/10.1007/s10295-017-1968-2
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 5 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Simultaneous consumption of pentose and hexose sugars: an optimal microbial phenotype for efficient fermentation of lignocellulosic biomass
journal, September 2010
- Kim, Jae-Han; Block, David E.; Mills, David A.
- Applied Microbiology and Biotechnology, Vol. 88, Issue 5
Pentose transport by the ruminal bacterium Butyrivibrio fibrisolvens
journal, October 1994
- Strobel, Herbert J.
- FEMS Microbiology Letters, Vol. 122, Issue 3
Regulation of endoglucanase gene (cmcax) expression in Acetobacter xylinum
journal, July 2008
- Kawano, Shin; Tajima, Kenji; Kono, Hiroyuki
- Journal of Bioscience and Bioengineering, Vol. 106, Issue 1
The Role of Bacterial Enhancer Binding Proteins as Specialized Activators of 54-Dependent Transcription
journal, August 2012
- Bush, M.; Dixon, R.
- Microbiology and Molecular Biology Reviews, Vol. 76, Issue 3
Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system.
journal, January 1989
- Saier, M. H.
- Microbiological Reviews, Vol. 53, Issue 1
The mechanisms of carbon catabolite repression in bacteria
journal, April 2008
- Deutscher, Josef
- Current Opinion in Microbiology, Vol. 11, Issue 2, p. 87-93
Isolation and identification of Alicyclobacillus acidocaldarius by 16S rDNA from mango juice and concentrate
journal, August 2005
- Gouws, Pieter A.; Gie, Lindy; Pretorius, Ashley
- International Journal of Food Science & Technology, Vol. 40, Issue 7
IMG/M: the integrated metagenome data management and comparative analysis system
journal, November 2011
- Markowitz, V. M.; Chen, I. -M. A.; Chu, K.
- Nucleic Acids Research, Vol. 40, Issue D1
Regulation of Carbon Catabolism in Bacillus Species
journal, October 2000
- Stülke, J.; Hillen, W.
- Annual Review of Microbiology, Vol. 54, Issue 1
Regulation of Expression of Cellulosomal Cellulase and Hemicellulase Genes in Clostridium cellulovorans
journal, October 2003
- Han, S. O.; Yukawa, H.; Inui, M.
- Journal of Bacteriology, Vol. 185, Issue 20
The complete genome of the crenarchaeon Sulfolobus solfataricus P2
journal, June 2001
- She, Q.; Singh, R. K.; Confalonieri, F.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 14, p. 7835-7840
Mechanisms for activating bacterial RNA polymerase
journal, September 2010
- Ghosh, Tamaswati; Bose, Daniel; Zhang, Xiaodong
- FEMS Microbiology Reviews, Vol. 34, Issue 5
Cyclic AMP regulates the biosynthesis of cellobiohydrolase in Cellulomonas flavigena growing in sugar cane bagasse
journal, August 2009
- Herrera-Herrera, Jesús Antonio; Pérez-Avalos, Odilia; Salgado, Luis M.
- Archives of Microbiology, Vol. 191, Issue 10
Transcriptome Analysis of Temporal Regulation of Carbon Metabolism by CcpA in <i>Bacillus subtilis</i> Reveals Additional Target Genes
journal, December 2006
- Lulko, Andrzej T.; Buist, Girbe; Kok, Jan
- Journal of Molecular Microbiology and Biotechnology, Vol. 12, Issue 1-2
Transcriptional regulation of pentose utilisation systems in the Bacillus/Clostridium group of bacteria
journal, December 2001
- Rodionov, Dmitry A.; Mironov, Andrey A.; Gelfand, Mikhail S.
- FEMS Microbiology Letters, Vol. 205, Issue 2
Simultaneous uptake and utilisation of glucose and xylose by Clostridium thermohydrosulfuricum
journal, May 1993
- Cook, Gregory M.; Janssen, Peter H.; Morgan, Hugh W.
- FEMS Microbiology Letters, Vol. 109, Issue 1
Complete genome sequence of Alicyclobacillus acidocaldarius type strain (104-IAT)
journal, January 2010
- Mavromatis, Konstantinos; Sikorski, Johannes; Lapidus, Alla
- Standards in Genomic Sciences, Vol. 2, Issue 1
AcpA, a member of the GPR1/FUN34/YaaH membrane protein family, is essential for acetate permease activity in the hyphal fungus Aspergillus nidulans
journal, May 2008
- Robellet, Xavier; Flipphi, Michel; Pégot, Sylvine
- Biochemical Journal, Vol. 412, Issue 3
Gene cloning, nucleotide sequence and biochemical properties of a cytoplasmic cyclomaltodextrinase (neopullulanase) from Alicyclobacillus acidocaldarius , reclassification of a group of enzymes
journal, February 2000
- Matzke, Jutta; Herrmann, Anja; Schneider, Erwin
- FEMS Microbiology Letters, Vol. 183, Issue 1
A Novel Thermoacidophilic Cellulase from Alicyclobacillus acidocaldarius
journal, September 2008
- Morana, A.; Esposito, A.; Maurelli, L.
- Protein & Peptide Letters, Vol. 15, Issue 9
Isolation and Characterization of Transposon-Insertional Mutants from Paenibacillus polymyxa E681 Altering the Biosynthesis of Indole-3-Acetic Acid
journal, February 2008
- Phi, Quyet Tien; Oh, Sang-Ho; Park, Yu-Mi
- Current Microbiology, Vol. 56, Issue 5
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003
- Bolstad, B. M.; Irizarry, R. A.; Astrand, M.
- Bioinformatics, Vol. 19, Issue 2
Comparative Sequence Analyses on the 16S rRNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, and Bacillus cycloheptanicus and Proposal for Creation of a New Genus, Alicyclobacillus gen. nov.
journal, April 1992
- Wisotzkey, J. D.; Jurtshuk, P.; Fox, G. E.
- International Journal of Systematic Bacteriology, Vol. 42, Issue 2
Cloning and sequencing of a gene encoding acidophilic amylase from Bacillus acidocaldarius
journal, October 1993
- Koivula, y.; Hemila, H.; Pakkanen, R.
- Journal of General Microbiology, Vol. 139, Issue 10
The Thermoanaerobacter Glycobiome Reveals Mechanisms of Pentose and Hexose Co-Utilization in Bacteria
journal, October 2011
- Lin, Lu; Song, Houhui; Tu, Qichao
- PLoS Genetics, Vol. 7, Issue 10
The DNA-binding domain as a functional indicator: the case of the AraC/XylS family of transcription factors
journal, August 2007
- Ibarra, J. Antonio; Pérez-Rueda, Ernesto; Segovia, Lorenzo
- Genetica, Vol. 133, Issue 1
Crystal Structures of A. acidocaldarius Endoglucanase Cel9A in Complex with Cello-Oligosaccharides: Strong −1 and −2 Subsites Mimic Cellobiohydrolase Activity
journal, November 2009
- Eckert, Kelvin; Vigouroux, Armelle; Lo Leggio, Leila
- Journal of Molecular Biology, Vol. 394, Issue 1
Signal sensory systems that impact σ 54 -dependent transcription
journal, May 2011
- Shingler, Victoria
- FEMS Microbiology Reviews, Vol. 35, Issue 3
Application of the hypervariable region of the 16S rDNA sequence as an index for the rapid identification of species in the genus Alicyclobacillus.
journal, January 2002
- Goto, Keiichi; Mochida, Kaoru; Asahara, Mika
- The Journal of General and Applied Microbiology, Vol. 48, Issue 5
A thermoacidophilic endoglucanase (CelB) from Alicyclobacillus acidocaldarius displays high sequence similarity to arabinofuranosidases belonging to family 51 of glycoside hydrolases
journal, August 2003
- Eckert, Kelvin; Schneider, Erwin
- European Journal of Biochemistry, Vol. 270, Issue 17, p. 3593-3602
Purification and characterization of highly thermostable α-amylase from thermophilic Alicyclobacillus acidocaldarius
journal, June 2010
- Satheesh kumar, G.; Chandra, M. Subhosh; Mallaiah, K. V.
- Biotechnology and Bioprocess Engineering, Vol. 15, Issue 3
H2 synthesis from pentoses and biomass in Thermotoga spp.
journal, October 2010
- Eriksen, Niels T.; Riis, Martin Leegaard; Holm, Nikolaj Kyndby
- Biotechnology Letters, Vol. 33, Issue 2
Occurrence of a thermoacidophilic cell-bound exo-pectinase inAlicyclobacillus acidocaldarius
journal, December 1998
- Ordoñez, R. G.; Morlon-Guyot, J.; Gasparian, S.
- Folia Microbiologica, Vol. 43, Issue 6
Alicyclobacilli from an unexplored geothermal soil in Antarctica: Mount Rittmann
journal, January 1998
- Nicolaus, Barbara; Improta, Roberta; Manca, Maria C.
- Polar Biology, Vol. 19, Issue 2
Characterization of a β-glycosidase from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius
journal, April 2006
- Lauro, Barbara Di; Rossi, Mosè; Moracci, Marco
- Extremophiles, Vol. 10, Issue 4, p. 301-310
Exploration, normalization, and summaries of high density oligonucleotide array probe level data
journal, April 2003
- Irizarry, Rafael A.; Hobbs, Bridget; Collin, Francois
- Biostatistics, Vol. 4, Issue 2, p. 249-264
Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination
journal, August 2002
- Atrih, Abdelmadjid; Foster, Simon J.; Moir, Anne
- Microbiology, Vol. 148, Issue 8
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
journal, August 2004
- Edgar, Robert C.
- BMC Bioinformatics, Vol. 5, Issue 1, p. 113
Absence of Diauxie during Simultaneous Utilization of Glucose and Xylose by Sulfolobus acidocaldarius
journal, January 2011
- Joshua, C. J.; Dahl, R.; Benke, P. I.
- Journal of Bacteriology, Vol. 193, Issue 6
Comparative analyses imply that the enigmatic sigma factor 54 is a central controller of the bacterial exterior
journal, August 2011
- Francke, Christof; Groot Kormelink, Tom; Hagemeijer, Yanick
- BMC Genomics, Vol. 12, Issue 1
Thermophilic hydrogen fermentation from Korean rice straw by Thermotoga neapolitana
journal, December 2010
- Nguyen, Tam-Anh D.; Kim, Kyoung-Rok; Kim, Mi Sun
- International Journal of Hydrogen Energy, Vol. 35, Issue 24
Determination of monosaccharide composition in plant fiber materials by capillary zone electrophoresis
journal, March 2008
- Rovio, Stella; Simolin, Helena; Koljonen, Krista
- Journal of Chromatography A, Vol. 1185, Issue 1
Molecular Analysis of the xylFGH Operon, Coding for Xylose ABC Transport, in Thermoanaerobacter ethanolicus
journal, April 2004
- Erbeznik, Milutin; Hudson, Sarah E.; Herrman, Adam B.
- Current Microbiology, Vol. 48, Issue 4
Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters
journal, March 2001
- Elferink, Marieke G. L.; Albers, Sonja-V.; Konings, Wil N.
- Molecular Microbiology, Vol. 39, Issue 6
Isolation and identification of species of Alicyclobacillus from orchard soil in the Western Cape, South Africa
journal, October 2007
- Groenewald, Willem H.; Gouws, Pieter A.; Witthuhn, R. Corli
- Extremophiles, Vol. 12, Issue 1
Confirmation and Elimination of Xylose Metabolism Bottlenecks in Glucose Phosphoenolpyruvate-Dependent Phosphotransferase System-Deficient Clostridium acetobutylicum for Simultaneous Utilization of Glucose, Xylose, and Arabinose
journal, September 2011
- Xiao, Han; Gu, Yang; Ning, Yuanyuan
- Applied and Environmental Microbiology, Vol. 77, Issue 22
Bacterial oligopeptide-binding proteins
journal, October 2003
- Monnet, V.
- Cellular and Molecular Life Sciences (CMLS), Vol. 60, Issue 10
Isolation and characterization of a new family 42 β-galactosidase from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius: Identification of the active site residues
journal, February 2008
- Di Lauro, Barbara; Strazzulli, Andrea; Perugino, Giuseppe
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1784, Issue 2, p. 292-301
Engineered Escherichia coli capable of co-utilization of cellobiose and xylose
journal, January 2012
- Vinuselvi, Parisutham; Lee, Sung Kuk
- Enzyme and Microbial Technology, Vol. 50, Issue 1
A Novel Lipase Belonging to the Hormone-sensitive Lipase Family Induced under Starvation to Utilize Stored Triacylglycerol in Mycobacterium tuberculosis
journal, January 2006
- Deb, C.
- Journal of Biological Chemistry, Vol. 281, Issue 7
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013
- Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
- Molecular Biology and Evolution, Vol. 30, Issue 12
A Two-Component System Regulates the Expression of an ABC Transporter for Xylo-Oligosaccharides in Geobacillus stearothermophilus
journal, December 2006
- Shulami, S.; Zaide, G.; Zolotnitsky, G.
- Applied and Environmental Microbiology, Vol. 73, Issue 3
Biosynthesis of the cyclohexanecarboxylic acid starter unit of .omega.-cyclohexyl fatty acids in Alicyclobacillus acidocaldarius
journal, June 1993
- Moore, Bradley S.; Poralla, Karl; Floss, Heinz G.
- Journal of the American Chemical Society, Vol. 115, Issue 12
Works referencing / citing this record:
A snapshot of microbial diversity and function in an undisturbed sugarcane bagasse pile
journal, February 2020
- Gebbie, Leigh; Dam, Tuan Tu; Ainscough, Rebecca
- BMC Biotechnology, Vol. 20, Issue 1