Comparison of single-molecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant clostridia

Brown, Steven D; Nagaraju, Shilpa; Utturkar, Sagar; De Tissera, Sashini; Segovia, Simón; Mitchell, Wayne; Land, Miriam L; Dassanayake, Asela; Köpke, Michael

doi:10.1186/1754-6834-7-40

Cited by 145Genomics and Phylogenetic StudiesMicrobial Metabolic Engineering and BioproductionBiofuel production and bioconversion

Comparison of single-molecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant clostridia

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Brown, Steven D, Nagaraju, Shilpa, Utturkar, Sagar, De Tissera, Sashini, Segovia, Simón, Mitchell, Wayne, Land, Miriam L, Dassanayake, Asela +1 more·2014·Biotechnology for Biofuels

DOI 10.1186/1754-6834-7-40PMC PMC4022347

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Abstract

BACKGROUND: Clostridium autoethanogenum strain JA1-1 (DSM 10061) is an acetogen capable of fermenting CO, CO2 and H2 (e.g. from syngas or waste gases) into biofuel ethanol and commodity chemicals such as 2,3-butanediol. A draft genome sequence consisting of 100 contigs has been published. RESULTS: A closed, high-quality genome sequence for C. autoethanogenum DSM10061 was generated using only the latest single-molecule DNA sequencing technology and without the need for manual finishing. It is assigned to the most complex genome classification based upon genome features such as repeats, prophage, nine copies of the rRNA gene operons. It has a low G + C content of 31.1%. Illumina, 454, Illumina/454 hybrid assemblies were generated and then compared to the draft and PacBio assemblies using summary statistics, CGAL, QUAST and REAPR bioinformatics tools and comparative genomic approaches. Assemblies based upon shorter read DNA technologies were confounded by the large number repeats and their size, which in the case of the rRNA gene operons were ~5 kb. CRISPR (Clustered Regularly Interspaced Short Paloindromic Repeats) systems among biotechnologically relevant Clostridia were classified and related to plasmid content and prophages. Potential associations between plasmid content and CRISPR systems may have implications for historical industrial scale Acetone-Butanol-Ethanol (ABE) fermentation failures and future large scale bacterial fermentations. While C. autoethanogenum contains an active CRISPR system, no such system is present in the closely related Clostridium ljungdahlii DSM 13528. A common prophage inserted into the Arg-tRNA shared between the strains suggests a common ancestor. However, C. ljungdahlii contains several additional putative prophages and it has more than double the amount of prophage DNA compared to C. autoethanogenum. Other differences include important metabolic genes for central metabolism (as an additional hydrogenase and the absence of a phophoenolpyruvate synthase) and substrate utilization pathway (mannose and aromatics utilization) that might explain phenotypic differences between C. autoethanogenum and C. ljungdahlii. CONCLUSIONS: Single molecule sequencing will be increasingly used to produce finished microbial genomes. The complete genome will facilitate comparative genomics and functional genomics and support future comparisons between Clostridia and studies that examine the evolution of plasmids, bacteriophage and CRISPR systems.

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Whole genome sequences have been elucidated for a range of acetogens including C. autoethanogenum, C. ljungdahlii, C. aceticum, M. thermoacetica, A. woodii, and E. limosum.
“These include elucidation of whole genome sequences for a range of acetogens including C. autoethanogenum (Brown et al., 2014; Humphreys et al., 2015; Utturkar et al., 2015), C. ljungdahlii (Köpke et al., 2010), C. aceticum (Poehlein et al., 2015), M. thermoacetica (Pierce et al., 2008), A. woodii (Poehlein et al., 2012), and E. limosum (Roh et al., 2011);”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Brown et al., 2014
Some acetogens such as C. autoethanogenum also have a native CRISPR system that has been shown to be actively transcribed.
“Some acetogens as C. autoethanogenum also have a native CRSIPR system, that has been shown to be actively transcribed (Brown et al., 2014).”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Brown et al., 2014

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Brown, S. D., Gilmour, C. C., Kucken, A. M., Wall, J. D., Elias, D. A., Brandt, C. C., Podar, M., Chertkov, O., Held, B., Bruce, D. C., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.00170-11 · Cited by 44 · see citing works
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Complete Genome Sequence of Clostridium acetobutylicum DSM 1731, a Solvent-Producing Strain with Multireplicon Genome Architecture
Bao, G., Wang, R., Zhu, Y., Dong, H., Mao, S., Zhang, Y., Chen, Z., Li, Y., & Ma, Y. (2011) · Journal of Bacteriology · doi:10.1128/jb.05596-11 · Cited by 42 · see citing works
Complete Genome Sequence of the Cellulolytic Thermophile Caldicellulosiruptor obsidiansis OB47 T
Elkins, J. G., Lochner, A., Hamilton-Brehm, S. D., Davenport, K. W., Podar, M., Brown, S. D., Land, M., Hauser, L., Klingeman, D. M., Raman, B., et al. (2010) · Journal of Bacteriology · doi:10.1128/jb.00950-10 · Cited by 39 · see citing works
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Draft Genome Sequences for Clostridium thermocellum Wild-Type Strain YS and Derived Cellulose Adhesion-Defective Mutant Strain AD2
Brown, S. D., Lamed, R., Morag, E., Borovok, I., Shoham, Y., Klingeman, D. M., Johnson, C. M., Yang, Z. K., Land, M., Utturkar, S. M., et al. (2012) · Journal of Bacteriology · doi:10.1128/jb.00473-12 · Cited by 31 · see citing works
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De Novo Assembly of the Streptomyces sp. Strain Mg1 Genome Using PacBio Single-Molecule Sequencing
Hoefler, B. C., Konganti, K., & Straight, P. D. (2013) · Genome Announcements · doi:10.1128/genomea.00535-13 · Cited by 30 · see citing works
Genome Sequence of the Autotrophic Acetogen Clostridium autoethanogenum JA1-1 Strain DSM 10061, a Producer of Ethanol from Carbon Monoxide
Bruno-Bárcena, J. M., Chinn, M. S., & Grunden, A. M. (2013) · Genome Announcements · doi:10.1128/genomea.00628-13 · Cited by 26 · see citing works
Complete Genome Sequence of the Solvent Producer Clostridium saccharobutylicum NCP262 (DSM 13864)
Poehlein, A., Hartwich, K., Krabben, P., Ehrenreich, A., Liebl, W., Dürre, P., Gottschalk, G., & Daniel, R. (2013) · Genome Announcements · doi:10.1128/genomea.00997-13 · Cited by 26 · see citing works
Genome Sequence of the Butanol Hyperproducer Clostridium saccharoperbutylacetonicum N1-4
del Cerro, C., Felpeto‐Santero, C., Rojas, A., Tortajada, M., Ramón, D., & García, J. L. (2013) · Genome Announcements · doi:10.1128/genomea.00070-13 · Cited by 21 · see citing works
Draft Genome Sequences for Two Metal-Reducing Pelosinus fermentans Strains Isolated from a Cr(VI)-Contaminated Site and for Type Strain R7
Brown, S. D., Podar, M., Klingeman, D. M., Johnson, C. M., Yang, Z. K., Utturkar, S. M., Land, M., Mosher, J. J., Hurt, R. A., Phelps, T. J., et al. (2012) · Journal of Bacteriology · doi:10.1128/jb.01174-12 · Cited by 20 · see citing works
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Draft Genome Sequence of Rhizobium sp. Strain PDO1-076, a Bacterium Isolated from Populus deltoides
Brown, S. D., Klingeman, D. M., Lu, T.-Y. S., Johnson, C. M., Utturkar, S. M., Land, M., Schadt, C. W., Doktycz, M. J., & Pelletier, D. A. (2012) · Journal of Bacteriology · doi:10.1128/jb.00198-12 · Cited by 18 · see citing works
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Draft Genome Sequence for Caulobacter sp. Strain OR37, a Bacterium Tolerant to Heavy Metals
Utturkar, S. M., Bollmann, A., Brzoska, R. M., Klingeman, D. M., Epstein, S. E., Palumbo, A. V., & Brown, S. D. (2013) · Genome Announcements · doi:10.1128/genomea.00322-13 · Cited by 14 · see citing works
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Influence of Carbon Source Pre-Adaptation on Clostridium ljungdahlii Growth and Product Formation
Tirado-Acevedo, O., Cotter, J. L., Chinn, M. S., & Grunden, A. M. (2011) · Journal of Bioprocessing & Biotechniques · doi:10.4172/2155-9821.s2-001 · Cited by 14 · see citing works
Draft Genome Sequence for Ralstonia sp. Strain OR214, a Bacterium with Potential for Bioremediation
Utturkar, S. M., Bollmann, A., Brzoska, R. M., Klingeman, D. M., Epstein, S. E., Palumbo, A. V., & Brown, S. D. (2013) · Genome Announcements · doi:10.1128/genomea.00321-13 · Cited by 13 · see citing works
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Draft Genome Sequences for Three Mercury-Methylating, Sulfate-Reducing Bacteria
Brown, S. D., Hurt, R. A., Gilmour, C. C., & Elias, D. A. (2013) · Genome Announcements · doi:10.1128/genomea.00618-13 · Cited by 7 · see citing works
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Reducing assembly complexity of microbial genomes with single-molecule sequencing
Koren, S., Harhay, G. P., Smith, T. P. L., Bono, J. L., Harhay, D. M., McVey, S., Radune, D., Bergman, N. H., & Phillippy, A. M. (2013) · Genome biology · doi:10.1186/gb-2013-14-9-r101 · Cited by 7 · see citing works
Complete Genome Sequence of the Cellulolytic Thermophile Clostridium thermocellum DSM1313
Feinberg, L. F., Foden, J. M., Barrett, T. F., Davenport, K. W., Bruce, D. G., Detter, C., Tapia, R., Han, C. S., Lapidus, A. L., Lucas, S. M., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.00322-11 · Cited by 2 · see citing works
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PacBio Sequencing and its Applications
Rhoads, A., & Au, K. F. (2015) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2015.08.002 · Cited by 2,338 · see citing works
Lysogeny in nature: mechanisms, impact and ecology of temperate phages
Howard‐Varona, C., Hargreaves, K. R., Abedon, S. T., & Sullivan, M. B. (2017) · The ISME Journal · doi:10.1038/ismej.2017.16 · Cited by 886 · see citing works
Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks
Liew, F., Martin, M. E., Tappel, R. C., Heijstra, B. D., Mihalcea, C., & Köpke, M. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00694 · Cited by 485 · see citing works
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One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly
Koren, S., & Phillippy, A. M. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.11.014 · Cited by 406 · see citing works
C1-carbon sources for chemical and fuel production by microbial gas fermentation
Dürre, P., & Eikmanns, B. J. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2015.03.008 · Cited by 242 · see citing works
Metabolic engineering of Clostridium autoethanogenum for selective alcohol production
Liew, F. E., Henstra, A. M., Köpke, M., Winzer, K., Simpson, S. D., & Minton, N. P. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.01.007 · Cited by 239 · see citing works
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Energy Conservation Associated with Ethanol Formation from H 2 and CO 2 in Clostridium autoethanogenum Involving Electron Bifurcation
Mock, J., Zheng, Y., Mueller, A. P., Ly, S., Tran, L., Segovia, S., Nagaraju, S., Köpke, M., Dürre, P., & Thauer, R. K. (2015) · Journal of Bacteriology · doi:10.1128/jb.00399-15 · Cited by 220 · see citing works
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Application of Next Generation Sequencing in Laboratory Medicine
Zhong, Y., Xu, F., Wu, J., Schubert, J. A., & Li, M. M. (2020) · Annals of Laboratory Medicine · doi:10.3343/alm.2021.41.1.25 · Cited by 216 · see citing works
Using gas mixtures of CO, CO 2 and H 2 as microbial substrates: the do's and don'ts of successful technology transfer from laboratory to production scale
Takors, R., Kopf, M., Mampel, J., Bluemke, W., Blombach, B., Eikmanns, B. J., Bengelsdorf, F. R., Weuster‐Botz, D., & Dürre, P. (2018) · Microbial Biotechnology · doi:10.1111/1751-7915.13270 · Cited by 192 · see citing works
Harnessing heterologous and endogenous CRISPR-Cas machineries for efficient markerless genome editing in Clostridium
Pyne, M. E., Bruder, M. R., Moo‐Young, M., Chung, D. A., & Chou, C.-H. P. (2016) · Scientific Reports · doi:10.1038/srep25666 · Cited by 175 · see citing works
Stepping on the Gas to a Circular Economy: Accelerating Development of Carbon-Negative Chemical Production from Gas Fermentation
Fackler, N., Heijstra, B. D., Rasor, B. J., Brown, H., Martin, J. P., Ni, Z., Shebek, K. M., Rosin, R. R., Simpson, S. D., Tyo, K. E. J., et al. (2021) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-120120-021122 · Cited by 169 · see citing works
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Bacterial Anaerobic Synthesis Gas (Syngas) and CO 2 + H 2 Fermentation
Bengelsdorf, F. R., Beck, M. H., Erz, C., Hoffmeister, S., Karl, M. M., Riegler, P., Wirth, S., Poehlein, A., Weuster‐Botz, D., & Dürre, P. (2018) · Advances in applied microbiology · doi:10.1016/bs.aambs.2018.01.002 · Cited by 164 · see citing works
Maintenance of ATP Homeostasis Triggers Metabolic Shifts in Gas-Fermenting Acetogens
Valgepea, K., Lemgruber, R. D. S. P., Meaghan, K., Palfreyman, R. W., Abdalla, T., Heijstra, B. D., Behrendorff, J. B. Y. H., Tappel, R. C., Köpke, M., Simpson, S. D., et al. (2017) · Cell Systems · doi:10.1016/j.cels.2017.04.008 · Cited by 162 · see citing works
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Low carbon fuels and commodity chemicals from waste gases – systematic approach to understand energy metabolism in a model acetogen
Marcellin, E., Behrendorff, J. B., Nagaraju, S., DeTissera, S., Segovia, S., Palfreyman, R. W., Daniell, J., Licona-Cassani, C., Quek, L.-E., Speight, R., et al. (2016) · Green Chemistry · doi:10.1039/c5gc02708j · Cited by 159 · see citing works
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Long-read, whole-genome shotgun sequence data for five model organisms
Kim, K. E., Peluso, P. S., Babayan, P., Yeadon, P. J., Yu, C. Y., Fisher, W. W., Chin, C.-S., Rapicavoli, N. A., Rank, D. R., Li, J., et al. (2014) · Scientific Data · doi:10.1038/sdata.2014.45 · Cited by 142 · see citing works
Genomics in the long-read sequencing era
van Dijk, E., Naquin, D., Gorrichon, K., Jaszczyszyn, Y., Ouazahrou, R., Thermes, C., & Hernandez, C. (2023) · Trends in Genetics · doi:10.1016/j.tig.2023.04.006 · Cited by 134 · see citing works
H2 drives metabolic rearrangements in gas-fermenting Clostridium autoethanogenum
Valgepea, K., Lemgruber, R. D. S. P., Abdalla, T., Binos, S., Takemori, N., Takemori, A., Tanaka, Y., Tappel, R. C., Köpke, M., Simpson, S. D., et al. (2018) · Biotechnology for Biofuels · doi:10.1186/s13068-018-1052-9 · Cited by 130 · see citing works
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Genome editing of Clostridium autoethanogenum using CRISPR/Cas9
Nagaraju, S., Davies, N., Walker, D. J. F., Köpke, M., & Simpson, S. D. (2016) · Biotechnology for Biofuels · doi:10.1186/s13068-016-0638-3 · Cited by 126 · see citing works
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Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities
Xu, Q., Resch, M. G., Podkaminer, K., Yang, S., Baker, J. O., Donohoe, B. S., Wilson, C. M., Klingeman, D. M., Olson, D. G., Decker, S. R., et al. (2016) · Science Advances · doi:10.1126/sciadv.1501254 · Cited by 125 · see citing works
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Arginine deiminase pathway provides ATP and boosts growth of the gas-fermenting acetogen Clostridium autoethanogenum
Valgepea, K., Loi, Q. K., Behrendorff, J. B. Y. H., Lemgruber, R. D. S. P., Plan, M. R., Hodson, M. P., Köpke, M., Nielsen, L. K., & Marcellin, E. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.04.007 · Cited by 118 · see citing works
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Industrial Acetogenic Biocatalysts: A Comparative Metabolic and Genomic Analysis
Bengelsdorf, F. R., Poehlein, A., Linder, S., Erz, C., Hummel, T., Hoffmeister, S., Daniel, R., & Dürre, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01036 · Cited by 112 · see citing works
Reconstruction of an Acetogenic 2,3-Butanediol Pathway Involving a Novel NADPH-Dependent Primary-Secondary Alcohol Dehydrogenase
Köpke, M., Gerth, M. L., Maddock, D. J., Mueller, A. P., Liew, F. E., Simpson, S. D., & Patrick, W. M. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.00301-14 · Cited by 111 · see citing works
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Traits of selected Clostridium strains for syngas fermentation to ethanol
Martin, M. E., Richter, H., Saha, S., & Angenent, L. T. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25827 · Cited by 111 · see citing works
Evaluation and validation ofde novoand hybrid assembly techniques to derive high-quality genome sequences
Utturkar, S. M., Klingeman, D. M., Land, M., Schadt, C. W., Doktycz, M. J., Pelletier, D. A., & Brown, S. D. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu391 · Cited by 108 · see citing works
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Insights into CO 2 Fixation Pathway of Clostridium autoethanogenum by Targeted Mutagenesis
Liew, F. E., Henstra, A. M., Winzer, K., Köpke, M., Simpson, S. D., & Minton, N. P. (2016) · mBio · doi:10.1128/mbio.00427-16 · Cited by 100 · see citing works
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Evidence for a Hexaheteromeric Methylenetetrahydrofolate Reductase in Moorella thermoacetica
Mock, J., Wang, S., Huang, H., Kahnt, J., & Thauer, R. K. (2014) · Journal of Bacteriology · doi:10.1128/jb.01839-14 · Cited by 99 · see citing works
Development of both type I–B and type II CRISPR/Cas genome editing systems in the cellulolytic bacterium Clostridium thermocellum
Walker, J. E., Lanahan, A. A., Zheng, T., Toruno, C., Lynd, L. R., Cameron, J. C., Olson, D. G., & Eckert, C. A. (2019) · Metabolic Engineering Communications · doi:10.1016/j.mec.2019.e00116 · Cited by 95 · see citing works
Valorization of C1 gases to value-added chemicals using acetogenic biocatalysts
Bae, J., Song, Y., Lee, H., Shin, J., Jin, S., Kang, S., & Cho, B. (2021) · Chemical Engineering Journal · doi:10.1016/j.cej.2021.131325 · Cited by 93 · see citing works
Gas fermentation: cellular engineering possibilities and scale up
Heijstra, B. D., Leang, C., & Juminaga, A. (2017) · Microbial Cell Factories · doi:10.1186/s12934-017-0676-y · Cited by 92 · see citing works
Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism
Yin, L., An, Y., Qu, J., Li, X., Zhang, Y., Dry, I. B., Wu, H., & Lu, J. (2017) · Scientific Reports · doi:10.1038/srep46553 · Cited by 84 · see citing works
Systems-level engineering and characterisation of Clostridium autoethanogenum through heterologous production of poly-3-hydroxybutyrate (PHB)
Lemgruber, R. D. S. P., Valgepea, K., Tappel, R. C., Behrendorff, J. B. Y. H., Palfreyman, R. W., Plan, M. R., Hodson, M. P., Simpson, S. D., Nielsen, L. K., Köpke, M., et al. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.01.003 · Cited by 83 · see citing works
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Whole genome sequence and manual annotation of Clostridium autoethanogenum, an industrially relevant bacterium
Humphreys, C. M., McLean, S., Schatschneider, S., Millat, T., Henstra, A. M., Annan, F. J., Breitkopf, R., Pander, B., Piatek, P., Rowe, P., et al. (2015) · BMC Genomics · doi:10.1186/s12864-015-2287-5 · Cited by 73 · see citing works
Impact of cyclic pH shifts on carbon monoxide fermentation to ethanol by Clostridium autoethanogenum
Abubackar, H. N., Fernández‐Naveira, Á., Veiga, M. C., & Kennes, C. (2016) · Fuel · doi:10.1016/j.fuel.2016.03.048 · Cited by 73 · see citing works
Extending CRISPR-Cas9 Technology from Genome Editing to Transcriptional Engineering in the Genus Clostridium
Bruder, M. R., Pyne, M. E., Moo‐Young, M., Chung, D. A., & Chou, C.-H. P. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.02128-16 · Cited by 73 · see citing works
Improved operating strategy for continuous fermentation of carbon monoxide to fuel-ethanol by clostridia
Abubackar, H. N., Bengelsdorf, F. R., Dürre, P., Veiga, M. C., & Kennes, C. (2016) · Applied Energy · doi:10.1016/j.apenergy.2016.02.021 · Cited by 72 · see citing works
Synthetic Biology on Acetogenic Bacteria for Highly Efficient Conversion of C1 Gases to Biochemicals
Jin, S., Bae, J., Song, Y., Pearcy, N., Shin, J., Kang, S., Minton, N. P., Soucaille, P., & Cho, B. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207639 · Cited by 72 · see citing works
Comparative analysis of high butanol tolerance and production in clostridia
Patáková, P., Kolek, J., Sedlář, K., Koščová, P., Branská, B., Kupkova, K., Paulová, L., & Provazník, I. (2017) · Biotechnology Advances · doi:10.1016/j.biotechadv.2017.12.004 · Cited by 72 · see citing works
Function of the CRISPR-Cas System of the Human Pathogen Clostridium difficile
Boudry, P., Semenova, E., Monot, M., Datsenko, K. A., Lopatina, A., Sekulović, O., Ospina-Bedoya, M., Fortier, L., Severinov, K., Dupuy, B., et al. (2015) · mBio · doi:10.1128/mbio.01112-15 · Cited by 71 · see citing works
Overcoming the energetic limitations of syngas fermentation
Molitor, B., Marcellin, E., & Angenent, L. T. (2017) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2017.10.003 · Cited by 71 · see citing works
Engineering Acetogenic Bacteria for Efficient One-Carbon Utilization
Lee, H., Bae, J., Jin, S., Kang, S., & Cho, B. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.865168 · Cited by 69 · see citing works
Completing bacterial genome assemblies: strategy and performance comparisons
Liao, Y.-C., Lin, S.-H., & Lin, H.-H. (2015) · Scientific Reports · doi:10.1038/srep08747 · Cited by 67 · see citing works
Fixation of CO2 and CO on a diverse range of carbohydrates using anaerobic, non-photosynthetic mixotrophy
Maru, B. T., Munasinghe, P. C., Gilary, H., Jones, S. W., & Tracy, B. P. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny039 · Cited by 65 · see citing works
Analysis of the Core Genome and Pan-Genome of Autotrophic Acetogenic Bacteria
Shin, J., Song, Y., Jeong, Y., & Cho, B. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01531 · Cited by 64 · see citing works
CoLoRMap: Correcting Long Reads by Mapping short reads
Haghshenas, E., Hach, F., Şahinalp, S. C., & Chauve, C. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw463 · Cited by 58 · see citing works
Rapid, multiplexed, whole genome and plasmid sequencing of foodborne pathogens using long-read nanopore technology
Taylor, T. L., Volkening, J. D., DeJesus, E., Simmons, M., Dimitrov, K. M., Tillman, G. E., Suarez, D. L., & Afonso, C. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-52424-x · Cited by 58 · see citing works
Ethanol Metabolism Dynamics in Clostridium ljungdahlii Grown on Carbon Monoxide
Liu, Z., Jia, D., Zhang, K.-D., Zhu, H., Zhang, Q., Jiang, W., Gu, Y., & Li, F. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.00730-20 · Cited by 54 · see citing works
Modeling a co-culture of Clostridium autoethanogenum and Clostridium kluyveri to increase syngas conversion to medium-chain fatty-acids
Benito-Vaquerizo, S., Diender, M., Olm, I. P., dos Santos, V. A. P. M., Schaap, P. J., Sousa, D. Z., & Diez, M. S. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.10.003 · Cited by 52 · see citing works
Advanced aspects of acetogens
Poehlein, A., Zeldes, B. M., Flaiz, M., Böer, T., Lüschen, A., Höfele, F., Baur, K. S., Molitor, B., Kröly, C., Wang, M., et al. (2024) · Bioresource Technology · doi:10.1016/j.biortech.2024.131913 · Cited by 51 · see citing works
Syngas Biorefinery and Syngas Utilization
Tissera, S. L. D., Köpke, M., Simpson, S. D., Humphreys, C. M., Minton, N. P., & Dürre, P. (2017) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2017_5 · Cited by 50 · see citing works
Self-citation
Development of a clostridia-based cell-free system for prototyping genetic parts and metabolic pathways
Krüger, A., Mueller, A. P., Rybnicky, G. A., Engle, N. L., Yang, Z. K., Tschaplinski, T. J., Simpson, S. D., Köpke, M., & Jewett, M. C. (2020) · Metabolic Engineering · doi:10.1016/j.ymben.2020.06.004 · Cited by 50 · see citing works
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Efficiency of PacBio long read correction by 2nd generation Illumina sequencing
Mahmoud, M., Żywicki, M., Twardowski, T., & Karlowski, W. M. (2017) · Genomics · doi:10.1016/j.ygeno.2017.12.011 · Cited by 49 · see citing works
Nitrate Feed Improves Growth and Ethanol Production of Clostridium ljungdahlii With CO2 and H2, but Results in Stochastic Inhibition Events
Klask, C.-M., Kliem-Kuster, N., Molitor, B., & Angenent, L. T. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00724 · Cited by 49 · see citing works
Gas channel rerouting in a primordial enzyme: Structural insights of the carbon-monoxide dehydrogenase/acetyl-CoA synthase complex from the acetogen Clostridium autoethanogenum
Lemaire, O. N., & Wagner, T. (2020) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2020.148330 · Cited by 47 · see citing works
Sequence data for Clostridium autoethanogenum using three generations of sequencing technologies
Utturkar, S. M., Klingeman, D. M., Bruno-Barcena, J. M., Chinn, M. S., Grunden, A. M., Köpke, M., & Brown, S. D. (2015) · Scientific Data · doi:10.1038/sdata.2015.14 · Cited by 46 · see citing works
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Genome-scale analysis of syngas fermenting acetogenic bacteria reveals the translational regulation for its autotrophic growth
Song, Y., Shin, J., Jin, S., Lee, J.-K., Kim, D. R., Kim, S. C., Cho, S., & Cho, B. (2018) · BMC Genomics · doi:10.1186/s12864-018-5238-0 · Cited by 45 · see citing works
Agricultural and Other Biotechnological Applications Resulting from Trophic Plant-Endophyte Interactions
Kuźniar, A., Włodarczyk, K., & Wolińska, A. (2019) · Agronomy · doi:10.3390/agronomy9120779 · Cited by 45 · see citing works
CRISPR Genome Editing Systems in the Genus Clostridium : a Timely Advancement
McAllister, K. N., & Sorg, J. A. (2019) · Journal of Bacteriology · doi:10.1128/jb.00219-19 · Cited by 43 · see citing works
Third generation sequencing technologies applied to diagnostic microbiology: benefits and challenges in applications and data analysis
Lavezzo, E., Barzon, L., Toppo, S., & Palù, G. (2016) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2016.1217158 · Cited by 42 · see citing works
Autotrophic adaptive laboratory evolution of the acetogen Clostridium autoethanogenum delivers the gas-fermenting strain LAbrini with superior growth, products, and robustness
Ingelman, H., Heffernan, J. K., Harris, A., Brown, S. D., Shaikh, K. M., Saqib, A. Y., Pinheiro, M. J., de Lima, L. A., Martinez, K. R., González-García, R. A., et al. (2024) · New Biotechnology · doi:10.1016/j.nbt.2024.06.002 · Cited by 41 · see citing works
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Biological conversion of carbon monoxide and hydrogen by anaerobic culture: Prospect of anaerobic digestion and thermochemical processes combination
Andreides, D., Fliegerova, K. O., Pokorná, D., & Zábranská, J. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107886 · Cited by 41 · see citing works
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Additional file 1: of Whole genome sequence and manual annotation of Clostridium autoethanogenum, an industrially relevant bacterium
Humphreys, C. M., McLean, S., Schatschneider, S., Millat, T., Henstra, A. M., Annan, F. J., Breitkopf, R., Pander, B., Piatek, P., Rowe, P., et al. (2015) · Figshare · doi:10.6084/m9.figshare.c.3624212_d5

Authors: Brown, S. D., Nagaraju, S., Utturkar, S., De Tissera, S., Segovia, S., Mitchell, W., Land, M. L., Dassanayake, A., & Köpke, M.
Affiliations: Oak Ridge National Laboratory (US)
LanzaTech (New Zealand) (NZ)
University of Tennessee at Knoxville (US)
Corresponding author: Brown, Steven D
Köpke, Michael
ORCID: Brown, Steven D
Nagaraju, Shilpa
Utturkar, Sagar
Land, Miriam L
Köpke, Michael
Venue: Biotechnology for Biofuels
Publisher: Springer Science and Business Media LLC
Published: 2014-03-21
Volume: 7
Issue: 1
Pages: 40-40
ISSN: 1754-6834 (ISSN-L)
DOI: 10.1186/1754-6834-7-40
PMC: PMC4022347
OpenAlex: W2151208862
Cited by: 145
References: 88
Citations by year: 2026: 5 · 2025: 9 · 2024: 6 · 2023: 7 · 2022: 11 · 2021: 10 · 2020: 9 · 2019: 13 · 2018: 13 · 2017: 18 · 2016: 18 · 2015: 18 · 2014: 8
FWCI: 8.48
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/2.0 (tdm)
creativecommons.org/licenses/by/2.0 (vor)
Locations: Biotechnology for Biofuels (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: U.S. Department of Energy (AC05-00OR22725, DE--AC05--00OR22725, DE-AC05?, under Contract DE-AC05-00OR22725, 00OR22725)
Battelle (DE-AC05- 00OR22725, AC05-00OR22725, DE-AC05)
UT-Battelle (DE-AC05, DEAC05-00OR22725, Contract DE-AC05-00OR22725, AC05-00OR22725)
Office of Science (DEAC05- 00OR22725, AC05-00OR22725)
Oak Ridge National Laboratory (AC05-00OR22725, DE-AC05-00OR22725)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Physical Sciences › Engineering › Biomedical Engineering › Biofuel production and bioconversion
Keywords: Clostridium autoethanogenum, Clostridium ljungdahlii, genome finishing, single-molecule sequencing, PacBio, hybrid sequencing, genome assembly comparison, CRISPR systems, prophages, plasmids, acetone-butanol-ethanol fermentation, acetogenic bacteria, hydrogenase, comparative genomics, industrial fermentation

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Comparison of single-molecule sequencing and hybrid approaches for finishing the genome of Clostridium autoethanogenum and analysis of CRISPR systems in industrial relevant clostridia

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