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Title: Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius

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. A. acidocaldarius grew while simultaneously metabolizing xylose and glucose, xylose and arabinose, and fructose and glucose, indicating CCR did not control carbon metabolism. Microarrays showed down-regulation of genes during growth on one sugar compared to two. Regulation occurred primarily in genes: 1) encoding regulators, 2) encoding enzymes for cell synthesis, and 3) encoding sugar transporters.

Authors:
ORCiD logo; ; ;
Publication Date:
Research Org.:
Idaho National Lab. (INL), Idaho Falls, ID (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1390430
Report Number(s):
PNNL-SA-119293
Journal ID: ISSN 1367-5435
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
Journal of Industrial Microbiology and Biotechnology
Additional Journal Information:
Journal Volume: 44; Journal Issue: 10; Journal ID: ISSN 1367-5435
Publisher:
Springer
Country of Publication:
United States
Language:
English

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. United States: 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. United States. doi:10.1007/s10295-017-1968-2.
Lee, Brady D., Apel, William A., DeVeaux, Linda C., and Sheridan, Peter P. Thu . "Concurrent metabolism of pentose and hexose sugars by the polyextremophile Alicyclobacillus acidocaldarius". United States. doi:10.1007/s10295-017-1968-2.
@article{osti_1390430,
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 = {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. A. acidocaldarius grew while simultaneously metabolizing xylose and glucose, xylose and arabinose, and fructose and glucose, indicating CCR did not control carbon metabolism. Microarrays showed down-regulation of genes during growth on one sugar compared to two. Regulation occurred primarily in genes: 1) encoding regulators, 2) encoding enzymes for cell synthesis, and 3) encoding sugar transporters.},
doi = {10.1007/s10295-017-1968-2},
journal = {Journal of Industrial Microbiology and Biotechnology},
issn = {1367-5435},
number = 10,
volume = 44,
place = {United States},
year = {2017},
month = {8}
}

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
  • DOI: 10.1007/s00253-010-2839-1

Pentose transport by the ruminal bacterium Butyrivibrio fibrisolvens
journal, October 1994


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
  • DOI: 10.1263/jbb.106.88

The mechanisms of carbon catabolite repression in bacteria
journal, April 2008


Isolation and identification of Alicyclobacillus acidocaldarius by 16S rDNA from mango juice and concentrate
journal, August 2005


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
  • DOI: 10.1093/nar/gkr975

Regulation of Carbon Catabolism in Bacillus Species
journal, October 2000


Regulation of Expression of Cellulosomal Cellulase and Hemicellulase Genes in Clostridium cellulovorans
journal, October 2003


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
  • DOI: 10.1073/pnas.141222098

Mechanisms for activating bacterial RNA polymerase
journal, September 2010


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
  • DOI: 10.1007/s00203-009-0502-y

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
  • DOI: 10.1159/000096463

Transcriptional regulation of pentose utilisation systems in the Bacillus/Clostridium group of bacteria
journal, December 2001


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
  • DOI: 10.1128/jb.01219-10

Simultaneous uptake and utilisation of glucose and xylose by Clostridium thermohydrosulfuricum
journal, May 1993


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
  • DOI: 10.4056/sigs.591104

An Expression-Driven Approach to the Prediction of Carbohydrate Transport and Utilization Regulons in the Hyperthermophilic Bacterium Thermotoga maritima
journal, November 2005


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
  • DOI: 10.1042/BJ20080124


journal, September 2008


A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003


Cloning and sequencing of a gene encoding acidophilic amylase from Bacillus acidocaldarius
journal, October 1993


The Thermoanaerobacter Glycobiome Reveals Mechanisms of Pentose and Hexose Co-Utilization in Bacteria
journal, October 2011


The DNA-binding domain as a functional indicator: the case of the AraC/XylS family of transcription factors
journal, August 2007


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
  • DOI: 10.1016/j.jmb.2009.08.060

Diversity and Versatility of the Thermotoga maritima Sugar Kinome
journal, August 2012

  • Rodionova, I. A.; Yang, C.; Li, X.
  • Journal of Bacteriology, Vol. 194, Issue 20
  • DOI: 10.1128/jb.01136-12

Signal sensory systems that impact σ 54 -dependent transcription
journal, May 2011


Regulation of Endo-Acting Glycosyl Hydrolases in the Hyperthermophilic Bacterium Thermotoga maritima Grown on Glucan- and Mannan-Based Polysaccharides
journal, February 2002

  • Chhabra, S. R.; Shockley, K. R.; Ward, D. E.
  • Applied and Environmental Microbiology, Vol. 68, Issue 2, p. 545-554
  • DOI: 10.1128/AEM.68.2.545-554.2002

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
  • DOI: 10.2323/jgam.48.243

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
  • DOI: 10.1007/s12257-009-0072-5

ABC transporters catalyzing carbohydrate uptake
journal, April 2001


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
  • DOI: 10.1007/s10529-010-0439-x

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
  • DOI: 10.1007/s003000050224

Characterization of a β-glycosidase from the thermoacidophilic bacterium Alicyclobacillus acidocaldarius
journal, April 2006


Exploration, normalization, and summaries of high density oligonucleotide array probe level data
journal, April 2003


Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination
journal, August 2002


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
  • DOI: 10.1016/S0022-2836(05)80360-2

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
  • DOI: 10.1186/1471-2164-12-385

Thermophilic hydrogen fermentation from Korean rice straw by Thermotoga neapolitana
journal, December 2010


Determination of monosaccharide composition in plant fiber materials by capillary zone electrophoresis
journal, March 2008


Effect of partial pressure of CO2 on the production of thermostable α-amylase and neutral protease by Bacillus caldolyticus
journal, February 2012


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
  • DOI: 10.1007/s00284-003-4202-6

Hyperthermophilic Thermotoga Species Differ with Respect to Specific Carbohydrate Transporters and Glycoside Hydrolases
journal, January 2012

  • Frock, Andrew D.; Gray, Steven R.; Kelly, Robert M.
  • Applied and Environmental Microbiology, Vol. 78, Issue 6
  • DOI: 10.1128/aem.07069-11

Sugar transport in Sulfolobus solfataricus is mediated by two families of binding protein-dependent ABC transporters
journal, March 2001


Isolation and identification of species of Alicyclobacillus from orchard soil in the Western Cape, South Africa
journal, October 2007


Bacterial oligopeptide-binding proteins
journal, October 2003


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
  • DOI: 10.1016/j.bbapap.2007.10.013

Engineered Escherichia coli capable of co-utilization of cellobiose and xylose
journal, January 2012


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
  • DOI: 10.1093/molbev/mst197

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
  • DOI: 10.1021/ja00065a043