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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
Open accessAbstract
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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![Figure 2 Inferred metabolism of C. autoethanogenum. Capital letters in brown denote enzymes. ATP, adenosine triphosphate, ADP, adenosine diphosphate; BDO, 2,3-butanediol; CO, carbon monoxide; CO2, carbon dioxide; FAD, flavin adenine dinucleotide; FADH2 FD_red, ferredoxin (reduced); FD_ox, ferredoxin (oxidized); G3P, 3-phosphoglycerate; GP, glycerone-phosphate; H3PO4, phosphate; NAD, nicotinamide adenine dinucleotide (oxidized); NADH, nicotinamide adenine dinucleotide (reduced); NADP, nicotinamide adenine dinucleotide phosphate (oxidized); NADPH, nicotinamide adenine dinucleotide phosphate (reduced); TCA, tricarboxcylic acid cycle. Note that reaction directionality has not been rigorously determined; in general, directionality is as reported in KEGG reactions. Acetyl-CoA (Wood-Ljungdahl) pathway – Reductive branch. W1 Bifunctional CO dehydrogenase/Acetyl-CoA synthase (CODH/ACS) CAETHG_1620-21, 1608-11, W2 Seleno formate dehydrogenase (Fdh) CAETHG_0084, 2789, W3 Non-seleno formate dehydrogenase (Fdh) CAETHG_2988, W4 Formyl-THF ligase (Fhs) CAETHG_1618, W5 Methenyl-THF cyclohydrolase (FchA) CAETHG_1617, W6 Methylene-THF dehydrogenase (FolD) CAETHG_1616, W7 Methylene-THF reductase (MetF) CAETHG_1614-15. Acetyl-CoA (Wood-Ljungdahl) pathway – Oxidative branch. C Monofunctional CO dehydrogenase CAETHG_3899, 3005, H1 Electron-bifurcating [FeFe] Hydrogenase (HytCBDE1AE2) CAETHG_2798, H2 Other [FeFe] hydrogenases (Hyd) CAETHG_0110, 0120, 1576, 3569, 3841, H3 [NiFe] hydrogenase (Hyd) CAETHG_0862, H4 Hydrogenase maturation factor (HypEDCF) CAETHG_0368-0371. Energy conservation. A F1FO ATPase (AtpIBEFHAGDC) CAETHG_2342-50, N Electron-bifurcating NADH-dependent Fd:NADP oxidoreductase (Nfn) CAETHG_1580, R Rnf complex (RnfCDGEAB) CAETHG_3227-32. Acetate fermentation pathway. Ac1 Phosphotransacetylase (Pta) CAETHG_3358, Ac2 Acetate kinase (Ack) CAETHG_3359. Ethanol fermentation pathway. E1 Bifunctional aldehyde/alcohol dehydrogenase (AdhE) CAETHG_3747, 3748, E2 Aldehyde:Fd oxidoreductase (AOR) CAETHG_0092, 0102, E3 Additional alcohol dehydrogenases (Adh) CAETHG_0555. 2,3-butanediol fermentation pathway. B1 Acetolactate synthase (AlsS) CAETHG_0124-25, 0406, 1740, B2 Acetolactate decarboxylase (BudA) CAETHG_2932, B3 2,3-butanediol dehydrogenase (Bdh) CAETHG_0385, Lactate fermentation pathway. L Lactate dehydrogenase (Ldh) CAETHG_1147. Central pyruvate metabolism. P1 Pyruvate:ferredoxin oxidoreductase (PFOR) CAETHG_0928, 3029, P2 Pyruvate, phosphate dikinase (PPDK) CAETHG_2055, 2909, P3 Pyruvate kinase (Pk) CAETHG_2440-41, P4 Pyruvate carboxylase (Pyc) CAETHG_1594, P5 PEP carboxykinase (PEPCK) CAETHG_2721, P5 Malic enzyme CAETHG_0605, 1055. Incomplete TCA cycle. T1 Citrate synthase CAETHG _2751, T2 Citrate lyase CAETHG_1052-54, 1898–1901, 2480-83, T3 Aconitase (Aco) CAETHG_1051, 2752, T4 Isocitrate dehydrogenase (Idh) CAETHG_2753, T5 Malate dehydrogenase (Mdh) CAETHG_1702, 2478, 2689, T6 Fumarase CAETHG_1902-03, 2062, 2479, T7 Fumarate reductase CAETHG_0344, 1032, 2961. Glycolysis/Gluconeogenesis. PTS Fructose phosphotransferase system (PTS) CAETHG_0142, 0676-73, G1 Fructokinase (Fk) /Fructose-6-phosphate isomerase CAETHG_0166, 0156, G2 1-phosphofructokinase (Pfk1) CAETHG_0143, G3 6-phosphofructokinase (Pfk6) CAETHG_648, 2439, G4 Fructose bisphosphate aldolase (Aldo) CAETHG_2382, G5 Triose-phosphate isomerase (Tpi) CAETHG_1758, G6 Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) CAETHG_1760, 3424, G7 Phosphoglycerate kinase (Pgk) CAETHG_1759, G8 Phosphoglycerate mutase (Pgm) CAETHG_712, 1757, G9 Enolase phosphopyruvate hydratase (Eno) CAETHG_1756.](/paper-figures/42d17f159ab74aefa7c1b65e733fd149/comparison-of-single-molecule-sequencing-and-hybrid-approaches-for-finishing-the-figure-2.jpg)
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“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
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“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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Metadata
- 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
- Venue
- Biotechnology for Biofuels
- Published
- 2014-03-21
- Volume
- 7
- Issue
- 1
- Pages
- 40-40
- ISSN
- 1754-6834 (ISSN-L)
- 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
- 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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