Transcriptional analysis of amino acid, metal ion, vitamin and carbohydrate uptake in butanol-producing Clostridium beijerinckii NRRL B-598
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31697692
PubMed Central
PMC6837493
DOI
10.1371/journal.pone.0224560
PII: PONE-D-19-22508
Knihovny.cz E-zdroje
- MeSH
- aminokyseliny genetika metabolismus MeSH
- butanoly metabolismus MeSH
- Clostridium beijerinckii genetika metabolismus MeSH
- fermentace MeSH
- genetická transkripce * MeSH
- kovy metabolismus MeSH
- metabolismus sacharidů genetika MeSH
- regulace genové exprese u bakterií genetika MeSH
- sacharidy genetika MeSH
- vitaminy genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- aminokyseliny MeSH
- butanoly MeSH
- kovy MeSH
- sacharidy MeSH
- vitaminy MeSH
In-depth knowledge of cell metabolism and nutrient uptake mechanisms can lead to the development of a tool for improving acetone-butanol-ethanol (ABE) fermentation performance and help to overcome bottlenecks in the process, such as the high cost of substrates and low production rates. Over 300 genes potentially encoding transport of amino acids, metal ions, vitamins and carbohydrates were identified in the genome of the butanol-producing strain Clostridium beijerinckii NRRL B-598, based on similarity searches in protein function databases. Transcriptomic data of the genes were obtained during ABE fermentation by RNA-Seq experiments and covered acidogenesis, solventogenesis and sporulation. The physiological roles of the selected 81 actively expressed transport genes were established on the basis of their expression profiles at particular stages of ABE fermentation. This article describes how genes encoding the uptake of glucose, iron, riboflavin, glutamine, methionine and other nutrients take part in growth, production and stress responses of C. beijerinckii NRRL B-598. These data increase our knowledge of transport mechanisms in solventogenic Clostridium and may be used in the selection of individual genes for further research.
Department of Biomedical Engineering Brno University of Technology Brno Czech Republic
Department of Biotechnology University of Chemistry and Technology Prague Prague Czech Republic
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Xing W, Xu G, Dong J, Han R, Ni Y. Novel dihydrogen-bonding deep eutectic solvents: Pretreatment of rice straw for butanol fermentation featuring enzyme recycling and high solvent yield. Chem Eng J. 2018;333: 712–720. 10.1016/j.cej.2017.09.176 DOI
Algayyim SJM, Wandel AP, Yusaf T, Hamawand I. Production and application of ABE as a biofuel. Renew Sustain Energy Rev. 2018;82: 1195–1214. 10.1016/j.rser.2017.09.082 DOI
Luo H, Zhang J, Wang H, Chen R, Shi Z, Li X, et al. Effectively enhancing acetone concentration and acetone/butanol ratio in ABE fermentation by a glucose/acetate co-substrate system incorporating with glucose limitation and C. acetobutylicum/S. cerevisiae co-culturing. Biochem Eng J. 2017;118: 132–142. 10.1016/j.bej.2016.12.003 DOI
Mascal M. Chemicals from biobutanol: Technologies and markets. Biofuel Bioprod Biorefin. 2012;6: 483–493. 10.1002/bbb.1328 DOI
Prat D, Pardigon O, Flemming HW, Letestu S, Ducandas V, Isnard P, et al. Sanofi’s solvent selection guide: A step toward more sustainable processes. Org Process Res Dev. 2013;17: 1517–1525. 10.1021/op4002565 DOI
Byrne FP, Jin S, Paggiola G, Petchey THM, Clark JH, Farmer TJ, et al. Tools and techniques for solvent selection: green solvent selection guides. Sustain Chem Process. 2016;4: 7 10.1186/s40508-016-0051-z DOI
Luo H, Ge L, Zhang J, Zhao Y, Ding J, Li Z, et al. Enhancing butanol production under the stress environments of co-culturing Clostridium acetobutylicum/Saccharomyces cerevisiae integrated with exogenous butyrate addition. PLoS One. 2015;10: e0141160 10.1371/journal.pone.0141160 PubMed DOI PMC
Wu YD, Xue C, Chen LJ, Bai FW. Effect of zinc supplementation on acetone-butanol-ethanol fermentation by Clostridium acetobutylicum. J Biotechnol. 2013;165: 18–21. 10.1016/j.jbiotec.2013.02.009 PubMed DOI
Liao Z, Suo Y, Xue C, Fu H, Wang J. Improving the fermentation performance of Clostridium acetobutylicum ATCC 824 by strengthening the VB1 biosynthesis pathway. Appl Microbiol Biotechnol. 2018;102: 8107–8119. 10.1007/s00253-018-9208-x PubMed DOI
Yang Y, Lang N, Yang G, Yang S, Jiang W, Gu Y. Improving the performance of solventogenic clostridia by reinforcing the biotin synthetic pathway. Metab Eng. 2016;35: 121–128. 10.1016/j.ymben.2016.02.006 PubMed DOI
Patakova P, Lipovsky J, Cizkova H, Fortova J, Rychtera M, Melzoch K. Exploitation of food feedstock and waste for production of biobutanol. Czech J Food Sci. 2009;27: 276–283. 10.2144/000113087 DOI
Mitchell WJ. Sugar uptake by the solventogenic clostridia. World J Microbiol Biotechnol. 2016;32: 32 10.1007/s11274-015-1981-4 PubMed DOI PMC
Servinsky MD, Kiel JT, Dupuy NF, Sund CJ. Transcriptional analysis of differential carbohydrate utilization by Clostridium acetobutylicum. Microbiology. 2010;156: 3478–91. 10.1099/mic.0.037085-0 PubMed DOI
Al Makishah NH, Mitchell WJ. Dual substrate specificity of an n-acetylglucosamine phosphotransferase system in Clostridium beijerinckii. Appl Environ Microbiol. 2013;79: 6712–6718. 10.1128/AEM.01866-13 PubMed DOI PMC
Reeve BWP, Reid SJ. Glutamate and histidine improve both solvent yields and the acid tolerance response of Clostridium beijerinckii NCP 260. J Appl Microbiol. 2016;120: 1271–1281. 10.1111/jam.13067 PubMed DOI
Sedlar K, Kolek J, Provaznik I, Patakova P. Reclassification of non-type strain Clostridium pasteurianum NRRL B-598 as Clostridium beijerinckii NRRL B-598. J Biotechnol. 2017;244: 1–3. 10.1016/j.jbiotec.2017.01.003 PubMed DOI
Sedlar K, Kolek J, Skutkova H, Branska B, Provaznik I, Patakova P. Complete genome sequence of Clostridium pasteurianum NRRL B-598, a non-type strain producing butanol. J Biotechnol. 2015;214: 113–114. 10.1016/j.jbiotec.2015.09.022 PubMed DOI
Kolek J, Sedlar K, Provaznik I, Patakova P. Dam and Dcm methylations prevent gene transfer into Clostridium pasteurianum NRRL B-598: development of methods for electrotransformation, conjugation, and sonoporation. Biotechnol Biofuels. 2016;9: 14 10.1186/s13068-016-0436-y PubMed DOI PMC
Kolek J, Branska B, Drahokoupil M, Patakova P, Melzoch K. Evaluation of viability, metabolic activity and spore quantity in clostridial cultures during ABE fermentation. FEMS Microbiol Lett. 2016;363: fnw031 10.1093/femsle/fnw031 PubMed DOI
Patakova P, Branska B, Sedlar K, Vasylkivska M, Jureckova K, Kolek J, et al. Acidogenesis, solventogenesis, metabolic stress response and life cycle changes in Clostridium beijerinckii NRRL B-598 at the transcriptomic level. Sci Rep. 2019;9: 1371 10.1038/s41598-018-37679-0 PubMed DOI PMC
Sedlar K, Koscova P, Vasylkivska M, Branska B, Kolek J, Kupkova K, et al. Transcription profiling of butanol producer Clostridium beijerinckii NRRL B-598 using RNA-Seq. BMC Genom. 2018;19: 415 10.1186/s12864-018-4805-8 PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30: 2114–2120. 10.1093/bioinformatics/btu170 PubMed DOI PMC
Kopylova E, Noe L, Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28: 3211–3217. 10.1093/bioinformatics/bts611 PubMed DOI
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41: 590–596. 10.1093/nar/gks1219 PubMed DOI PMC
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29: 15–21. 10.1093/bioinformatics/bts635 PubMed DOI PMC
Liao Y, Smyth GK, Shi W. FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30: 923–930. 10.1093/bioinformatics/btt656 PubMed DOI
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550 10.1186/s13059-014-0550-8 PubMed DOI PMC
Robinson MD, McCarthy DJ, Smyth GK. EdgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26: 139–140. 10.1093/bioinformatics/btp616 PubMed DOI PMC
Bateman A, Martin MJ, O’Donovan C, Magrane M, Apweiler R, Alpi E, et al. UniProt: A hub for protein information. Nucleic Acids Res. 2015;43: D204–D212. 10.1093/nar/gku989 PubMed DOI PMC
Mitchell AL, Attwood TK, Babbitt PC, Blum M, Bork P, Bridge A, et al. InterPro in 2019: Improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res. 2019;47: D351–D360. 10.1093/nar/gky1100 PubMed DOI PMC
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019;47: D427–D432. 10.1093/nar/gky995 PubMed DOI PMC
Gish W, States DJ. Identification of protein coding regions by database similarity search. Nat Genet. 1993;3: 266–272. 10.1038/ng0393-266 PubMed DOI
Saxena J, Tanner RS. Optimization of a corn steep medium for production of ethanol from synthesis gas fermentation by Clostridium ragsdalei. World J Microbiol Biotechnol. 2012;28: 1553–1561. 10.1007/s11274-011-0959-0 PubMed DOI
Soni BK, Soucaille P, Goma G. Continuous acetone-butanol fermentation: a global approach for the improvement in the solvent productivity in synthetic medium. Appl Microbiol Biotechnol. 1987;25: 317–321. 10.1007/bf00252540 DOI
Nguyen NPT, Raynaud C, Meynial-Salles I, Soucaille P. Reviving the Weizmann process for commercial n-butanol production. Nat Commun. 2018;9: 3682 10.1038/s41467-018-05661-z PubMed DOI PMC
Long S, Jones DT, Woods DR. Sporulation of Clostridium acetobutylicum P262 in a defined medium. Appl Environ Microbiol. 1983;45: 1389–1393. PubMed PMC
Storari M, Kulli S, Wüthrich D, Bruggmann R, Berthoud H, Arias-Roth E. Genomic approach to studying nutritional requirements of Clostridium tyrobutyricum and other Clostridia causing late blowing defects. Food Microbiol. 2016;59: 213–223. 10.1016/j.fm.2016.05.013 PubMed DOI
Jiao S, Zhang Y, Wan C, Lv J, Du R, Zhang R, et al. Transcriptional analysis of degenerate strain Clostridium beijerinckii DG-8052 reveals a pleiotropic response to CaCO(3)-associated recovery of solvent production. Sci Rep. 2016;6: 38818 10.1038/srep38818 PubMed DOI PMC
Alsaker K V., Paredes C, Papoutsakis ET. Metabolite stress and tolerance in the production of biofuels and chemicals: Gene-expression-based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum. Biotechnol Bioeng. 2010;105: 1131–1147. 10.1002/bit.22628 PubMed DOI
Amador-Noguez D, Brasg IA, Feng X-J, Roquet N, Rabinowitz JD. Metabolome remodeling during the acidogenic-solventogenic transition in Clostridium acetobutylicum. Appl Environ Microbiol. 2011;77: 7984–7997. 10.1128/AEM.05374-11 PubMed DOI PMC
Alsaker K V, Papoutsakis ET. Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum. J Bacteriol. 2005;187: 7103–7118. 10.1128/JB.187.20.7103-7118.2005 PubMed DOI PMC
Poudel S, Giannone RJ, Rodriguez M, Raman B, Martin MZ, Engle NL, et al. Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass. Biotechnol Biofuels. 2017;10: 14 10.1186/s13068-016-0697-5 PubMed DOI PMC
Henson MA, Phalak P. In silico analysis of Clostridium difficile biofilm metabolism and treatment. IFAC-PapersOnLine. 2016;49: 153–158. 10.1016/j.ifacol.2016.12.118 DOI
Larocque M, Chenard T, Najmanovich R. A curated C. difficile strain 630 metabolic network: prediction of essential targets and inhibitors. BMC Syst Biol. 2014;8: 117 10.1186/s12918-014-0117-z PubMed DOI PMC
Heluane H, Dagher MRE, Bruno-Barcena JM. Meta-analysis and functional validation of nutritional requirements of solventogenic clostridia growing under butanol stress conditions and coutilization of D-glucose and D-xylose. Appl Environ Microbiol. 2011;77: 4473–4485. 10.1128/AEM.00116-11 PubMed DOI PMC
Luo H, Ge L, Zhang J, Ding J, Chen R, Shi Z. Enhancing acetone biosynthesis and acetone–butanol–ethanol fermentation performance by co-culturing Clostridium acetobutylicum/Saccharomyces cerevisiae integrated with exogenous acetate addition. Bioresour Technol. 2016;200: 111–120. 10.1016/j.biortech.2015.09.116 PubMed DOI
Neumann-Schaal M, Hofmann JD, Will SE, Schomburg D. Time-resolved amino acid uptake of Clostridium difficile 630Δerm and concomitant fermentation product and toxin formation. BMC Microbiol. 2015;15: 281 10.1186/s12866-015-0614-2 PubMed DOI PMC
Durre P. Physiologyand sporulation in Clostridium. Microbiol Spectr. 2014;2: 315–329. 10.1128/microbiolspec.tbs-0010-2012 PubMed DOI
Eisenstadt E. Potassium content during growth and sporulation in Bacillus subtilis. J Bacteriol. 1972;112: 264–267. PubMed PMC
Wu YD, Xue C, Chen LJ, Wan HH, Bai FW. Transcriptional analysis of micronutrient zinc-associated response for enhanced carbohydrate utilization and earlier solventogenesis in Clostridium acetobutylicum. Sci Rep. 2015;5: 16598 10.1038/srep16598 PubMed DOI PMC
Winzer K, Lorenz K, Durre P. Acetate kinase from Clostridium acetobutylicum: A highly specific enzyme that is actively transcribed during acidogenesis and solventogenesis. Microbiology. 1997;143: 3279–3286. 10.1099/00221287-143-10-3279 PubMed DOI
Zhao X, Xing D, Liu B, Lu L, Zhao J, Ren N. The effects of metal ions and L-cysteine on hydA gene expression and hydrogen production by Clostridium beijerinckii RZF-1108. Int J Hydrogen Energy. 2012;37: 13711–13717. 10.1016/j.ijhydene.2012.02.144 DOI
Chin HL, Chen ZS, Chou CP. Fedbatch operation using Clostridium acetobutylicum suspension culture as biocatalyst for enhancing hydrogen production. Biotechnol Prog. 2003;19: 383–388. 10.1021/bp0200604 PubMed DOI
Bao MD, Su HJ, Tan TW. Dark fermentative bio-hydrogen production: Effects of substrate pre-treatment and addition of metal ions or L-cysteine. Fuel. 2013;112: 38–44. 10.1016/j.fuel.2013.04.063 DOI
Wu H, Wang C, Chen P, He A-Y, Xing F-X, Kong X-P, et al. Effects of pH and ferrous iron on the coproduction of butanol and hydrogen by Clostridium beijerinckii IB4. Int J Hydrogen Energy. 2017;42: 6547–6555. 10.1016/j.ijhydene.2017.02.094 DOI
Serio AW, Pechter KB, Sonenshein AL. Bacillus subtilis aconitase is required for efficient late-sporulation gene expression. J Bacteriol. 2006;188: 6396–6405. 10.1128/JB.00249-06 PubMed DOI PMC
Wu YD, Xue C, Chen LJ, Yuan WJ, Bai FW. Improvements of metabolites tolerance in Clostridium acetobutylicum by micronutrient zinc supplementation. Biotechnol Bioprocess Eng. 2016;21: 60–67. 10.1007/s12257-015-0583-1 DOI
Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN. Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genom. 2009;10: 78 10.1186/1471-2164-10-78 PubMed DOI PMC
Paredes CJ, Rigoutsos I, Papoutsakis T. Transcriptional organization of the Clostridium acetobutylicum genome. Nucleic Acids Res. 2004;32: 1973–1981. 10.1093/nar/gkh509 PubMed DOI PMC
Jaehme M, Slotboom DJ. Diversity of membrane transport proteins for vitamins in bacteria and archaea. Biochim Biophys Acta—Gen Subj. 2015;1850: 565–576. 10.1016/j.bbagen.2014.05.006 PubMed DOI
Maret W, Wedd A. Binding, transport and storage of metal ions in biological cells. Cambridge: The Royal Society of Chemistry; 2014. 10.1039/9781849739979 DOI
Shukla G, Thakur V. Biohydrogen production from rice mill wastes by Clostridium acetobutylicum NCIM 2877. World J Eng. 2015;12: 383–390. 10.1260/1708-5284.12.4.383 DOI
Zhang Y, Ezeji TC. Transcriptional analysis of Clostridium beijerinckii NCIMB 8052 to elucidate role of furfural stress during acetone butanol ethanol fermentation. Biotechnol Biofuels. 2013;6: 66 10.1186/1754-6834-6-66 PubMed DOI PMC
Hönicke D, Janssen H, Grimmler C, Ehrenreich A, Lütke-Eversloh T. Global transcriptional changes of Clostridium acetobutylicum cultures with increased butanol: acetone ratios. N Biotechnol. 2012;29: 485–493. 10.1016/j.nbt.2012.01.001 PubMed DOI
Worst DJ, Gerrits MM, Vandenbroucke-Grauls CMJE, Kusters JG. Helicobacter pylori ribBA-mediated riboflavin production is involved in iron acquisition. J Bacteriol. 1998;180: 1473–1479. PubMed PMC
Crossley RA, Gaskin DJH, Holmes K, Mulholland F, Wells JM, Kelly DJ, et al. Riboflavin biosynthesis is associated with assimilatory ferric reduction and iron acquisition by Campylobacter jejuni. Appl Environ Microbiol. 2007;73: 7819–7825. 10.1128/AEM.01919-07 PubMed DOI PMC
Von Canstein H, Ogawa J, Shimizu S, Lloyd JR. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol. 2008;74: 615–623. 10.1128/AEM.01387-07 PubMed DOI PMC
Rodionov DA, Li X, Rodionova IA, Yang C, Sorci L, Dervyn E, et al. Transcriptional regulation of NAD metabolism in bacteria: Genomic reconstruction of NiaR (YrxA) regulon. Nucleic Acids Res. 2008;36: 2032–2046. 10.1093/nar/gkn046 PubMed DOI PMC
Li T, Yan Y, He J. Reducing cofactors contribute to the increase of butanol production by a wild-type Clostridium sp. strain BOH3. Bioresour Technol. 2014;155: 220–228. 10.1016/j.biortech.2013.12.089 PubMed DOI
Mitchell WJ. The phosphotransferase system in solventogenic clostridia. J Mol Microbiol Biotechnol. 2015;25: 129–142. 10.1159/000375125 PubMed DOI
Shi Y, Li Y-X, Li Y-Y. Large number of phosphotransferase genes in the Clostridium beijerinckii NCIMB 8052 genome and the study on their evolution. BMC Bioinformatics. 2010;11: S9 10.1186/1471-2105-11-S11-S9 PubMed DOI PMC
Tangney M, Mitchell WJ. Characterisation of a glucose phosphotransferase system in Clostridium acetobutylicum ATCC 824. Appl Microbiol Biotechnol. 2007;74: 398–405. 10.1007/s00253-006-0679-9 PubMed DOI
Wang Y, Li X, Blaschek HP. Effects of supplementary butyrate on butanol production and the metabolic switch in Clostridium beijerinckii NCIMB 8052: genome-wide transcriptional analysis with RNA-Seq. Biotechnol Biofuels. 2013;6: 138 10.1186/1754-6834-6-138 PubMed DOI PMC
Wang Y, Li X, Mao Y, Blaschek HP. Genome-wide dynamic transcriptional profiling in Clostridium beijerinckii NCIMB 8052 using single-nucleotide resolution RNA-Seq. BMC Genom. 2012;13: 102 10.1186/1471-2164-13-102 PubMed DOI PMC
Seo S-O, Janssen H, Magis A, Wang Y, Lu T, Price ND, et al. Genomic, transcriptional, and phenotypic analysis of the glucose derepressed Clostridium beijerinckii mutant exhibiting acid crash phenotype. Biotechnol J. 2017;12: 1700182 10.1002/biot.201700182 PubMed DOI
Shi Z, Blaschek HP. Transcriptional analysis of Clostridium beijerinckii NCIMB 8052 and the hyper-butanol-producing mutant BA101 during the shift from acidogenesis to solventogenesis. Appl Environ Microbiol. 2008;74: 7709–7714. 10.1128/AEM.01948-08 PubMed DOI PMC
Zhang L, Leyn SA, Gu Y, Jiang W, Rodionov DA, Yang C. Ribulokinase and transcriptional regulation of arabinose metabolism in Clostridium acetobutylicum. J Bacteriol. 2012;194: 1055–1064. 10.1128/JB.06241-11 PubMed DOI PMC
Sun Z, Chen Y, Yang C, Yang S, Gu Y, Jiang W. A novel three-component system-based regulatory model for D-xylose sensing and transport in Clostridium beijerinckii. Mol Microbiol. 2015;95: 576–589. 10.1111/mmi.12894 PubMed DOI
Mitchell WJ. Physiology of carbohydrate to solvent conversion by Clostridia. Adv Microb Physiol. 1997;39: 31–130. 10.1016/S0065-2911(08)60015-6 PubMed DOI