The Complete Genome Sequence of Hyperthermophile Dictyoglomus turgidum DSM 6724™ Reveals a Specialized Carbohydrate Fermentor
Abstract
In this study we report the complete genome sequence of the chemoorganotrophic, extremely thermophilic bacterium, Dictyoglomus turgidum, which is a Gram negative, strictly anaerobic bacterium. D. turgidum and D. thermophilum together form the Dictyoglomi phylum. The two Dictyoglomus genomes are highly syntenic, and both are distantly related to Caldicellulosiruptor spp. D. turgidum is able to grow on a wide variety of polysaccharide substrates due to significant genomic commitment to glycosyl hydrolases, 16 of which were cloned and expressed in our study. The GH5, GH10, and GH42 enzymes characterized in this study suggest that D. turgidum can utilize most plant-based polysaccharides except crystalline cellulose. The DNA polymerase I enzyme was also expressed and characterized. The pure enzyme showed improved amplification of long PCR targets compared to Taq polymerase. The genome contains a full complement of DNA modifying enzymes, and an unusually high copy number (4) of a new, ancestral family of polB type nucleotidyltransferases designated as MNT (minimal nucleotidyltransferases). Considering its optimal growth at 72°C, D. turgidum has an anomalously low G+C content of 39.9% that may account for the presence of reverse gyrase, usually associated with hyperthermophiles.
- Authors:
-
- C5-6 Technologies LLC, Fitchburg, WI (United States); Univ. of Wisconsin, Madison, WI (United States)
- Univ. of Wisconsin, Madison, WI (United States); Lucigen Corp., Middleton, WI (United States)
- Univ. of Maryland, Baltimore, MD (United States)
- Univ. of Wisconsin, Madison, WI (United States); Varigen Biosciences Corp., Madison, WI (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Energy Efficiency and Renewable Energy (EERE)
- OSTI Identifier:
- 1373560
- Alternate Identifier(s):
- OSTI ID: 1466828
- Grant/Contract Number:
- FC02-07ER64494; AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Volume: 7; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Dictyoglomus turgidum; thermophile; biomass degradation; phage; Dictyoglomi; DNA polymerase; glucanase; reverse gyrase
Citation Formats
Brumm, Phillip J., Gowda, Krishne, Robb, Frank T., and Mead, David A. The Complete Genome Sequence of Hyperthermophile Dictyoglomus turgidum DSM 6724™ Reveals a Specialized Carbohydrate Fermentor. United States: N. p., 2016.
Web. doi:10.3389/fmicb.2016.01979.
Brumm, Phillip J., Gowda, Krishne, Robb, Frank T., & Mead, David A. The Complete Genome Sequence of Hyperthermophile Dictyoglomus turgidum DSM 6724™ Reveals a Specialized Carbohydrate Fermentor. United States. https://doi.org/10.3389/fmicb.2016.01979
Brumm, Phillip J., Gowda, Krishne, Robb, Frank T., and Mead, David A. Tue .
"The Complete Genome Sequence of Hyperthermophile Dictyoglomus turgidum DSM 6724™ Reveals a Specialized Carbohydrate Fermentor". United States. https://doi.org/10.3389/fmicb.2016.01979. https://www.osti.gov/servlets/purl/1373560.
@article{osti_1373560,
title = {The Complete Genome Sequence of Hyperthermophile Dictyoglomus turgidum DSM 6724™ Reveals a Specialized Carbohydrate Fermentor},
author = {Brumm, Phillip J. and Gowda, Krishne and Robb, Frank T. and Mead, David A.},
abstractNote = {In this study we report the complete genome sequence of the chemoorganotrophic, extremely thermophilic bacterium, Dictyoglomus turgidum, which is a Gram negative, strictly anaerobic bacterium. D. turgidum and D. thermophilum together form the Dictyoglomi phylum. The two Dictyoglomus genomes are highly syntenic, and both are distantly related to Caldicellulosiruptor spp. D. turgidum is able to grow on a wide variety of polysaccharide substrates due to significant genomic commitment to glycosyl hydrolases, 16 of which were cloned and expressed in our study. The GH5, GH10, and GH42 enzymes characterized in this study suggest that D. turgidum can utilize most plant-based polysaccharides except crystalline cellulose. The DNA polymerase I enzyme was also expressed and characterized. The pure enzyme showed improved amplification of long PCR targets compared to Taq polymerase. The genome contains a full complement of DNA modifying enzymes, and an unusually high copy number (4) of a new, ancestral family of polB type nucleotidyltransferases designated as MNT (minimal nucleotidyltransferases). Considering its optimal growth at 72°C, D. turgidum has an anomalously low G+C content of 39.9% that may account for the presence of reverse gyrase, usually associated with hyperthermophiles.},
doi = {10.3389/fmicb.2016.01979},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {Tue Dec 20 00:00:00 EST 2016},
month = {Tue Dec 20 00:00:00 EST 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
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:
MicrobesOnline: an integrated portal for comparative and functional genomics
journal, November 2009
- Dehal, P. S.; Joachimiak, M. P.; Price, M. N.
- Nucleic Acids Research, Vol. 38, Issue suppl_1, p. D396-D400
Cloning and nucleotide sequence of a heat-stable amylase gene from an anaerobic thermophile, Dictyoglomus thermophilum
journal, May 1988
- Fukusumi, Shoji; Kamizono, Akito; Horinouchi, Sueharu
- European Journal of Biochemistry, Vol. 174, Issue 1
High abundance of heterotrophic prokaryotes in hydrothermal springs of the Azores as revealed by a network of 16S rRNA gene-based methods
journal, May 2013
- Sahm, Kerstin; John, Patrick; Nacke, Heiko
- Extremophiles, Vol. 17, Issue 4
Thermaerobacter marianensis gen. nov., sp. nov., an aerobic extremely thermophilic marine bacterium from the 11000 m deep Mariana Trench
journal, April 1999
- Takai, K.; Inoue, A.; Horikoshi, K.
- International Journal of Systematic Bacteriology, Vol. 49, Issue 2
Using the MEROPS Database for Proteolytic Enzymes and Their Inhibitors and Substrates
journal, December 2014
- Rawlings, Neil D.; Barrett, Alan J.; Bateman, Alex
- Current Protocols in Bioinformatics, Vol. 48, Issue 1
Anaerobaculum thermoterrenum gen. nov., sp. nov., a Novel, Thermophilic Bacterium Which Ferments Citrate
journal, January 1997
- Rees, G. N.; Patel, B. K. C.; Grassia, G. S.
- International Journal of Systematic Bacteriology, Vol. 47, Issue 1
Conservation of Eubacterial Replicases
journal, June 2005
- Wijffels, Gene; Dalrymple, Brian; Kongsuwan, Kritaya
- IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Vol. 57, Issue 6
The phylogenetic position of Dictyoglomus thermophilum based on 16S rRNA sequence analysis
journal, March 1993
- Love, C. A.; Patel, B. K. C.; Ludwig, W.
- FEMS Microbiology Letters, Vol. 107, Issue 2-3
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes
journal, February 2014
- Kim, M.; Oh, H. -S.; Park, S. -C.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2
A novel thermostable polymerase for RNA and DNA loop-mediated isothermal amplification (LAMP)
journal, August 2014
- Chander, Yogesh; Koelbl, Jim; Puckett, Jamie
- Frontiers in Microbiology, Vol. 5
RNAmmer: consistent and rapid annotation of ribosomal RNA genes
journal, April 2007
- Lagesen, Karin; Hallin, Peter; Rødland, Einar Andreas
- Nucleic Acids Research, Vol. 35, Issue 9
CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats
journal, May 2007
- Grissa, I.; Vergnaud, G.; Pourcel, C.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Bacterial genomes: what they teach us about cellulose degradation
journal, November 2013
- Brumm, Phillip J.
- Biofuels, Vol. 4, Issue 6
Archaeal DNA Replication
journal, November 2014
- Kelman, Lori M.; Kelman, Zvi
- Annual Review of Genetics, Vol. 48, Issue 1
Sequencing, Cloning, and High-Level Expression of the pfp Gene, Encoding a PPi-Dependent Phosphofructokinase from the Extremely Thermophilic Eubacterium Dictyoglomus thermophilum
journal, August 2000
- Ding, Y. -H. R.; Ronimus, R. S.; Morgan, H. W.
- Journal of Bacteriology, Vol. 182, Issue 16
SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011
- Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
- Nature Methods, Vol. 8, Issue 10
Cloning and expression in Escherichia coli of two additional amylase genes of a strictly anaerobic thermophile, Dictyoglomus thermophilum, and their nucleotide sequences with extremely low guanine-plus-cytosine contents
journal, September 1988
- Horinouchi, Sueharu; Fukusumi, Shoji; Ohshima, Toyoji
- European Journal of Biochemistry, Vol. 176, Issue 2
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997
- Lowe, Todd M.; Eddy, Sean R.
- Nucleic Acids Research, Vol. 25, Issue 5
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
Expansion of the BioCyc collection of pathway/genome databases to 160 genomes
journal, October 2005
- Karp, P. D.
- Nucleic Acids Research, Vol. 33, Issue 19
Automated Genome Annotation and Metabolic Model Reconstruction in the SEED and Model SEED
book, January 2013
- Devoid, Scott; Overbeek, Ross; DeJongh, Matthew
- Methods in Molecular Biology
Thermophilic bacterial DNA polymerases with reverse-transcriptase activity
journal, June 2004
- Griffiths, Kate; Shandilya, Harini; Flynn, Elizabeth K.
- Extremophiles, Vol. 8, Issue 3
‘That which does not kill us only makes us stronger’: the role of carbon monoxide in thermophilic microbial consortia
journal, May 2009
- Techtmann, Stephen M.; Colman, Albert S.; Robb, Frank T.
- Environmental Microbiology, Vol. 11, Issue 5
Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities
journal, March 1998
- Ewing, Brent; Green, Phil
- Genome Research, Vol. 8, Issue 3
The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008
- Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
- BMC Genomics, Vol. 9, Issue 1, Article No. 75
Complete Genome Sequence of Thermus aquaticus Y51MC23
journal, October 2015
- Brumm, Phillip J.; Monsma, Scott; Keough, Brendan
- PLOS ONE, Vol. 10, Issue 10
Heterologous expression and characterization of a novel thermo-halotolerant endoglucanase Cel5H from Dictyoglomus thermophilum
journal, August 2013
- Shi, Runrun; Li, Zhimin; Ye, Qin
- Bioresource Technology, Vol. 142
Using MUMmer to Identify Similar Regions in Large Sequence Sets
journal, January 2003
- Delcher, Arthur L.; Salzberg, Steven L.; Phillippy, Adam M.
- Current Protocols in Bioinformatics, Vol. 00, Issue 1
Characterization of a recombinant cellobiose 2-epimerase from Dictyoglomus turgidum that epimerizes and isomerizes β-1,4- and α-1,4-gluco-oligosaccharides
journal, July 2012
- Kim, Jung-Eun; Kim, Yeong-Su; Kang, Lin-Woo
- Biotechnology Letters, Vol. 34, Issue 11
DNA repair in hyperthermophilic and hyperradioresistant microorganisms
journal, June 2015
- Ishino, Yoshizumi; Narumi, Issay
- Current Opinion in Microbiology, Vol. 25
Rfam: an RNA family database
journal, January 2003
- Griffiths-Jones, S.
- Nucleic Acids Research, Vol. 31, Issue 1
DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history
journal, April 1999
- Aravind, L.
- Nucleic Acids Research, Vol. 27, Issue 7
Comparative Geochemical and Microbiological Characterization of Two Thermal Pools in the Uzon Caldera, Kamchatka, Russia
journal, November 2011
- Burgess, Elizabeth A.; Unrine, Jason M.; Mills, Gary L.
- Microbial Ecology, Vol. 63, Issue 3
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002
- Katoh, K.
- Nucleic Acids Research, Vol. 30, Issue 14
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes
journal, September 2005
- Overbeek, R.
- Nucleic Acids Research, Vol. 33, Issue 17
Biodiversity of Thermophilic Prokaryotes with Hydrolytic Activities in Hot Springs of Uzon Caldera, Kamchatka (Russia)
journal, October 2008
- Kublanov, I. V.; Perevalova, A. A.; Slobodkina, G. B.
- Applied and Environmental Microbiology, Vol. 75, Issue 1
Tandem-repeat protein domains across the tree of life
journal, January 2015
- Jernigan, Kristin K.; Bordenstein, Seth R.
- PeerJ, Vol. 3
IslandPath: aiding detection of genomic islands in prokaryotes
journal, February 2003
- Hsiao, W.; Wan, I.; Jones, S. J.
- Bioinformatics, Vol. 19, Issue 3
Sequence analysis of GerM and SpoVS, uncharacterized bacterial ‘sporulation’ proteins with widespread phylogenetic distribution
journal, June 2008
- Rigden, Daniel J.; Galperin, Michael Y.
- Bioinformatics, Vol. 24, Issue 16
Isolation and characterization of a strictly xylan-degrading Dictyoglomus from a man-made, thermophilic anaerobic environment
journal, December 1991
- Mathrani, IndraM.; Ahring, BirgitteK.
- Archives of Microbiology, Vol. 157, Issue 1
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
Thermophilic and alkalophilic xylanases from several Dictyoglomus isolates
journal, October 1992
- Mathrani, IndraMadan; Ahring, BirgitteKi�r
- Applied Microbiology and Biotechnology, Vol. 38, Issue 1
Taxonomic note: necessary correction of specific and subspecific epithets according to Rules 12c and 13b of the International Code of Nomenclature of Bacteria (1990 Revision)
journal, July 1998
- Euzeby, J. P.
- International Journal of Systematic Bacteriology, Vol. 48, Issue 3
Hemicellulases and auxiliary enzymes for improved conversion of lignocellulosic biomass to monosaccharides
journal, January 2011
- Gao, Dahai; Uppugundla, Nirmal; Chundawat, Shishir PS
- Biotechnology for Biofuels, Vol. 4, Issue 1
Isolation of an extremely thermophilic chemoorganotrophic anaerobe similar to Dictyoglomus thermophilum from new zealand hot springs
journal, January 1987
- Patel, B. K.; Morgan, H. W.; Wiegel, J.
- Archives of Microbiology, Vol. 147, Issue 1
Consed: A Graphical Tool for Sequence Finishing
journal, March 1998
- Gordon, David; Abajian, Chris; Green, Phil
- Genome Research, Vol. 8, Issue 3
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011
- Tamura, K.; Peterson, D.; Peterson, N.
- Molecular Biology and Evolution, Vol. 28, Issue 10
Veillonella, Firmicutes: Microbes disguised as Gram negatives
journal, December 2013
- Vesth, Tammi; Ozen, Aslı; Andersen, Sandra C.
- Standards in Genomic Sciences, Vol. 9, Issue 3
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
PHAST and RPHAST: phylogenetic analysis with space/time models
journal, December 2010
- Hubisz, M. J.; Pollard, K. S.; Siepel, A.
- Briefings in Bioinformatics, Vol. 12, Issue 1
Whole-genome comparison clarifies close phylogenetic relationships between the phyla Dictyoglomi and Thermotogae
journal, November 2011
- Nishida, Hiromi; Beppu, Teruhiko; Ueda, Kenji
- Genomics, Vol. 98, Issue 5
Molecular characterization of a thermostable l-fucose isomerase from Dictyoglomus turgidum that isomerizes l-fucose and d-arabinose
journal, September 2012
- Hong, Seung-Hye; Lim, Yu-Ri; Kim, Yeong-Su
- Biochimie, Vol. 94, Issue 9
Molecular analysis of microbial diversity in the Zavarzin Spring, Uzon Caldera, Kamchatka
journal, April 2011
- Gumerov, V. M.; Mardanov, A. V.; Beletsky, A. V.
- Microbiology, Vol. 80, Issue 2
Comparative Metagenomics of Eight Geographically Remote Terrestrial Hot Springs
journal, February 2015
- Menzel, Peter; Gudbergsdóttir, Sóley Ruth; Rike, Anne Gunn
- Microbial Ecology, Vol. 70, Issue 2
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases
journal, November 2013
- Caspi, Ron; Altman, Tomer; Billington, Richard
- Nucleic Acids Research, Vol. 42, Issue D1
Genomic analysis of six new Geobacillus strains reveals highly conserved carbohydrate degradation architectures and strategies
journal, May 2015
- Brumm, Phillip J.; De Maayer, Pieter; Mead, David A.
- Frontiers in Microbiology, Vol. 6
PHAST: A Fast Phage Search Tool
journal, June 2011
- Zhou, Y.; Liang, Y.; Lynch, K. H.
- Nucleic Acids Research, Vol. 39, Issue suppl
Diversity of Thermophilic Anaerobes
journal, March 2008
- Wagner, Isaac D.; Wiegel, Juergen
- Annals of the New York Academy of Sciences, Vol. 1125, Issue 1
Anaerobic transformation of carbon monoxide by microbial communities of Kamchatka hot springs
journal, March 2011
- Kochetkova, Tatiana V.; Rusanov, Igor I.; Pimenov, Nikolay V.
- Extremophiles, Vol. 15, Issue 3
Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers
journal, January 2006
- Brochier-Armanet, Céline; Forterre, Patrick
- Archaea, Vol. 2, Issue 2
Sequencing and Expression of a β-Mannanase Gene from the Extreme Thermophile Dictyoglomus thermophilum Rt46B.1, and Characteristics of the Recombinant Enzyme
journal, December 1999
- Gibbs, Moreland D.
- Current Microbiology, Vol. 39, Issue 6
Characterization of a recombinant l-rhamnose isomerase from Dictyoglomus turgidum and its application for l-rhamnulose production
journal, October 2012
- Kim, Yeong-Su; Shin, Kyung-Chul; Lim, Yu-Ri
- Biotechnology Letters, Vol. 35, Issue 2
Cloning, sequencing, and expression of a xylanase gene from the extreme thermophile Dictyoglomus thermophilum Rt46B.1 and activity of the enzyme on fiber-bound substrate.
journal, January 1995
- Gibbs, M. D.; Reeves, R. A.; Bergquist, P. L.
- Applied and environmental microbiology, Vol. 61, Issue 12
Cloning of the xynB Gene fromDictyoglomus thermophilum Rt46B.1 and Action of the Gene Product on Kraft Pulp
journal, May 1998
- Morris, Daniel D.; Gibbs, Moreland D.; Chin, Charles W. J.
- Applied and Environmental Microbiology, Vol. 64, Issue 5
Whole-genome comparison clarifies close phylogenetic relationships between the phyla Dictyoglomi and Thermotogae
journal, November 2011
- Nishida, Hiromi; Beppu, Teruhiko; Ueda, Kenji
- Genomics, Vol. 98, Issue 5
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases
journal, November 2013
- Caspi, Ron; Altman, Tomer; Billington, Richard
- Nucleic Acids Research, Vol. 42, Issue D1
Purification and Characterization ofThermotoga maritima Endonuclease IV, a Thermostable Apurinic/Apyrimidinic Endonuclease and 3′-Repair Diesterase
journal, May 1999
- Haas, Brian J.; Sandigursky, Margarita; Tainer, John A.
- Journal of Bacteriology, Vol. 181, Issue 9
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
Works referencing / citing this record:
Complete genome sequence of Rhodothermaceae bacterium RA with cellulolytic and xylanolytic activities
journal, August 2018
- Liew, Kok Jun; Teo, Seng Chong; Shamsir, Mohd Shahir
- 3 Biotech, Vol. 8, Issue 8
The Evolution of Reverse Gyrase Suggests a Nonhyperthermophilic Last Universal Common Ancestor
journal, September 2019
- Catchpole, Ryan J.; Forterre, Patrick
- Molecular Biology and Evolution, Vol. 36, Issue 12