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Proteomic analyses of the phase transition from acidogenesis to solventogenesis using solventogenic and non-solventogenic Clostridium acetobutylicum strains

  • Genomics, transcriptomics, proteomics
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Abstract

The fermentation carried out by the solvent-producing bacterium, Clostridium acetobutylicum, is characterized by two distinct phases: acidogenic and solventogenic phases. Understanding the cellular physiological changes occurring during the phase transition in clostridial fermentation is important for the enhanced production of solvents. To identify protein changes upon entry to stationary phase where solvents are typically produced, we herein analyzed the proteomic profiles of the parental wild type C. acetobutylicum strains, ATCC 824, the non-solventogenic strain, M5 that has lost the solventogenic megaplasmid pSOL1, and the synthetic simplified alcohol forming strain, M5 (pIMP1E1AB) expressing plasmid-based CoA-transferase (CtfAB) and aldehyde/alcohol dehydrogenase (AdhE1). A total of 68 protein spots, corresponding to 56 unique proteins, were unambiguously identified as being differentially present after the phase transitions in the three C. acetobutylicum strains. In addition to changes in proteins known to be involved in solventogenesis (AdhE1 and CtfB), we identified significant alterations in enzymes involved in sugar transport and metabolism, fermentative pathway, heat shock proteins, translation, and amino acid biosynthesis upon entry into the stationary phase. Of these, four increased proteins (AdhE1, CAC0233, CtfB and phosphocarrier protein HPr) and six decreased proteins (butyrate kinase, ferredoxin:pyruvate oxidoreductase, phenylalanyl-tRNA synthetase, adenylosuccinate synthase, pyruvate kinase and valyl-tRNA synthetase) showed similar patterns in the two strains capable of butanol formation. Interestingly, significant changes of several proteins by post-translational modifications were observed in the solventogenic phase. The proteomic data from this study will improve our understanding on how cell physiology is affected through protein levels patterns in clostridia.

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References

  • Alsaker KV, Papoutsakis ET (2005) Transcriptional program of early sporulation and stationary-phase events in Clostridium acetobutylicum. J Bacteriol 187:7103–7118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alsaker KV, Paredes C, Papoutsakis ET (2010) 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 105:1131–1147

    CAS  PubMed  Google Scholar 

  • Altschul SF, Wootton JC, Gertz EM, Agarwala R, Morgulis A, Schaffer AA, Yu YK (2005) Protein database searches using compositionally adjusted substitution matrices. FEBS J 272:5101–5109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Amador-Noguez D, Brasg IA, Feng XJ, Roquet N, Rabinowitz JD (2011) Metabolome remodeling during the acidogenic–solventogenic transition in Clostridium acetobutylicum. Appl Environ Microbiol 77:7984–7997

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bachrach G, Banai M, Fishman Y, Bercovier H (1997) Delayed-type hypersensitivity activity of the Brucella L7/L12 ribosomal protein depends on posttranslational modification. Infect Immun 65:267–271

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bahl H, Muller H, Behrens S, Joseph H, Narberhaus F (1995) Expression of heat shock genes in Clostridium acetobutylicum. FEMS Microbiol Rev 17:341–348

    Article  CAS  PubMed  Google Scholar 

  • Bai X, Ji Z (2012) Phosphoproteomic investigation of a solvent producing bacterium Clostridium acetobutylicum. Appl Microbiol Biotechnol 95:201–211

    Article  CAS  PubMed  Google Scholar 

  • Balodimos IA, Rapaport E, Kashket ER (1990) Protein phosphorylation in response to stress in Clostridium acetobutylicum. Appl Environ Microbiol 56:2170–2173

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bruckner R, Titgemeyer F (2002) Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett 209:141–148

    Article  CAS  PubMed  Google Scholar 

  • Cary JW, Petersen DJ, Papoutsakis ET, Bennett GN (1990) Cloning and expression of Clostridium acetobutylicum ATCC 824 acetoacetyl-coenzyme A:acetate/butyrate:coenzyme A-transferase in Escherichia coli. Appl Environ Microbiol 56:1576–1583

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi SJ, Lee J, Jang YS, Park JH, Lee SY, Kim IH (2012) Effects of nutritional enrichment on the production of acetone–butanol–ethanol (ABE) by Clostridium acetobutylicum. J Microbiol 50:1063–1066

    Article  CAS  PubMed  Google Scholar 

  • Clark SW, Bennett GN, Rudolph FB (1989) Isolation and characterization of mutants of Clostridium acetobutylicum ATCC 824 deficient in acetoacetyl-coenzyme A:acetate/butyrate:coenzyme A transferase (EC 2.8.3.9) and in other solvent pathway enzymes. Appl Environ Microbiol 55:970–976

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cooksley CM, Zhang Y, Wang H, Redl S, Winzer K, Minton NP (2012) Targeted mutagenesis of the Clostridium acetobutylicum acetone–butanol–ethanol fermentation pathway. Metab Eng 14:630–641

    Article  CAS  PubMed  Google Scholar 

  • Cornillot E, Nair RV, Papoutsakis ET, Soucaille P (1997) The genes for butanol and acetone formation in Clostridium acetobutylicum ATCC 824 reside on a large plasmid whose loss leads to degeneration of the strain. J Bacteriol 179:5442–5447

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crown SB, Indurthi DC, Ahn WS, Choi J, Papoutsakis ET, Antoniewicz MR (2011) Resolving the TCA cycle and pentose–phosphate pathway of Clostridium acetobutylicum ATCC 824: isotopomer analysis, in vitro activities and expression analysis. Biotechnol J 6:300–305

    Article  CAS  PubMed  Google Scholar 

  • Desai RP, Papoutsakis ET (1999) Antisense RNA strategies for metabolic engineering of Clostridium acetobutylicum. Appl Environ Microbiol 65:936–945

    CAS  PubMed Central  PubMed  Google Scholar 

  • Deutscher J, Francke C, Postma PW (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70:939–1031

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Durre P (2007) Biobutanol: an attractive biofuel. Biotechnol J 2:1525–1534

    Article  PubMed  Google Scholar 

  • Fischer RJ, Helms J, Durre P (1993) Cloning, sequencing, and molecular analysis of the sol operon of Clostridium acetobutylicum, a chromosomal locus involved in solventogenesis. J Bacteriol 175:6959–6969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Green EM (2011) Fermentative production of butanol—the industrial perspective. Curr Opin Biotechnol 22:337–343

    Article  CAS  PubMed  Google Scholar 

  • Green EM, Boynton ZL, Harris LM, Rudolph FB, Papoutsakis ET, Bennett GN (1996) Genetic manipulation of acid formation pathways by gene inactivation in Clostridium acetobutylicum ATCC 824. Microbiology 142(Pt 8):2079–2086

    Article  CAS  PubMed  Google Scholar 

  • Grimmler C, Janssen H, Kraubetae D, Fischer RJ, Bahl H, Durre P, Liebl W, Ehrenreich A (2011) Genome-wide gene expression analysis of the switch between acidogenesis and solventogenesis in continuous cultures of Clostridium acetobutylicum. J Mol Microbiol Biotechnol 20:1–15

    Article  CAS  PubMed  Google Scholar 

  • Gu Y, Jiang Y, Wu H, Liu X, Li Z, Li J, Xiao H, Shen Z, Dong H, Yang Y, Li Y, Jiang W, Yang S (2011) Economical challenges to microbial producers of butanol: feedstock, butanol ratio and titer. Biotechnol J 6:1348–1357

    Article  CAS  PubMed  Google Scholar 

  • Haendeler J (2006) Thioredoxin-1 and posttranslational modifications. Antioxid Redox Signal 8:1723–1728

    Article  CAS  PubMed  Google Scholar 

  • Han M-J, Jeong KJ, Yoo J-S, Lee SY (2003) Engineering Escherichia coli for increased productivity of serine-rich proteins based on proteome profiling. Appl Environ Microbiol 69:5772–5781

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hanson KG, Steinhauer K, Reizer J, Hillen W, Stulke J (2002) HPr kinase/phosphatase of Bacillus subtilis: expression of the gene and effects of mutations on enzyme activity, growth and carbon catabolite repression. Microbiology 148:1805–1811

    CAS  PubMed  Google Scholar 

  • Harris LM, Desai RP, Welker NE, Papoutsakis ET (2000) Characterization of recombinant strains of the Clostridium acetobutylicum butyrate kinase inactivation mutant: need for new phenomenological models for solventogenesis and butanol inhibition? Biotechnol Bioeng 67:1–11

    Article  CAS  PubMed  Google Scholar 

  • Husemann MH, Papoutsakis ET (1988) Solventogenesis in Clostridium acetobutylicum fermentations related to carboxylic acid and proton concentrations. Biotechnol Bioeng 32:843–852

    Article  CAS  PubMed  Google Scholar 

  • Hutkins RW, Kashket ER (1986) Phosphotransferase activity in Clostridium acetobutylicum from acidogenic and solventogenic phases of growth. Appl Environ Microbiol 51:1121–1123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jang Y-S, Lee J, Malaviya A, Seung DY, Cho JH, Lee SY (2012a) Butanol production from renewable biomass: rediscovery of metabolic pathways and metabolic engineering. Biotechnol J 7:186–198

    Article  CAS  PubMed  Google Scholar 

  • Jang Y-S, Lee JY, Lee J, Park JH, Im JA, Eom M-H, Lee J, Lee S-H, Song H, Cho J-H, Seung DY, Lee SY (2012b) Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. mBio 3(5):e00314–12

  • Jang Y-S, Park JM, Choi S, Choi YJ, Seung DY, Cho JH, Lee SY (2012c) Engineering of microorganisms for the production of biofuels and perspectives based on systems metabolic engineering approaches. Biotechnol Adv 30:989–1000

    Article  CAS  PubMed  Google Scholar 

  • Jang YS, Woo HM, Im JA, Kim IH, Lee SY (2013) Metabolic engineering of Clostridium acetobutylicum for enhanced production of butyric acid. Appl Microbiol Biotechnol 97:9355–9363

    Article  CAS  PubMed  Google Scholar 

  • Janssen H, Doring C, Ehrenreich A, Voigt B, Hecker M, Bahl H, Fischer RJ (2010) A proteomic and transcriptional view of acidogenic and solventogenic steady-state cells of Clostridium acetobutylicum in a chemostat culture. Appl Microbiol Biotechnol 87:2209–2226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones DT, Woods DR (1986) Acetone–butanol fermentation revisited. Microbiol Rev 50:484–524

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones SW, Paredes CJ, Tracy B, Cheng N, Sillers R, Senger RS, Papoutsakis ET (2008) The transcriptional program underlying the physiology of clostridial sporulation. Genome Biol 9:R114

    Article  PubMed Central  PubMed  Google Scholar 

  • Kirschner M (2006) n-Butanol. Chemical Market Reporter, 30 Jan–5 Feb, ABI/INFORM Global; p 42

  • Kuit W, Minton NP, Lopez-Contreras AM, Eggink G (2012) Disruption of the acetate kinase (ack) gene of Clostridium acetobutylicum results in delayed acetate production. Appl Microbiol Biotechnol 94:729–741

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lee JW, Lee SY, Song H, Yoo J-S (2006) The proteome of Mannheimia succiniciproducens, a capnophilic rumen bacterium. Proteomics 6:3550–3566

    Article  CAS  PubMed  Google Scholar 

  • Lee SY, Park JH, Jang SH, Nielsen LK, Kim J, Jung KS (2008) Fermentative butanol production by Clostridia. Biotechnol Bioeng 101:209–228

    Article  CAS  PubMed  Google Scholar 

  • Lee JY, Jang YS, Lee J, Papoutsakis ET, Lee SY (2009) Metabolic engineering of Clostridium acetobutylicum M5 for highly selective butanol production. Biotechnol J 4:1432–1440

    Article  CAS  PubMed  Google Scholar 

  • Lehmann D, Honicke D, Ehrenreich A, Schmidt M, Weuster-Botz D, Bahl H, Lutke-Eversloh T (2012) Modifying the product pattern of Clostridium acetobutylicum: physiological effects of disrupting the acetate and acetone formation pathways. Appl Microbiol Biotechnol 94:743–754

    Article  CAS  PubMed  Google Scholar 

  • Mao S, Luo Y, Zhang T, Li J, Bao G, Zhu Y, Chen Z, Zhang Y, Li Y, Ma Y (2010) Proteome reference map and comparative proteomic analysis between a wild type Clostridium acetobutylicum DSM 1731 and its mutant with enhanced butanol tolerance and butanol yield. J Proteome Res 9:3046–3061

    Article  CAS  PubMed  Google Scholar 

  • Mao S, Jia K, Zhang Y, Li Y (2012) Use of proteomic tools in microbial engineering for biofuel production. In: Cheng Q (ed) Microbial metabolic engineering. Vol. 834. Springer, New York, pp 137–151

    Chapter  Google Scholar 

  • Mermelstein LD, Welker NE, Bennett GN, Papoutsakis ET (1992) Expression of cloned homologous fermentative genes in Clostridium acetobutylicum ATCC 824. Biotechnology 10:190–195

    Article  CAS  PubMed  Google Scholar 

  • Millat T, Janssen H, Bahl H, Fischer RJ, Wolkenhauer O (2013a) Integrative modelling of pH-dependent enzyme activity and transcriptomic regulation of the acetone–butanol–ethanol fermentation of Clostridium acetobutylicum in continuous culture. Microb Biotechnol 6:526–539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Millat T, Janssen H, Thorn GJ, King JR, Bahl H, Fischer RJ, Wolkenhauer O (2013b) A shift in the dominant phenotype governs the pH-induced metabolic switch of Clostridium acetobutylicumin phosphate-limited continuous cultures. Appl Microbiol Biotechnol 97:6451–6466

    Article  CAS  PubMed  Google Scholar 

  • Nicolaou SA, Gaida SM, Papoutsakis ET (2010) A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: from biofuels and chemicals, to biocatalysis and bioremediation. Metab Eng 12:307–331

    Article  CAS  PubMed  Google Scholar 

  • Nolling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, Gibson R, Lee HM, Dubois J, Qiu D, Hitti J, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR (2001) Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183:4823–4838

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Papoutsakis ET (2008) Engineering solventogenic clostridia. Curr Opin Biotechnol 19:420–429

    Article  CAS  PubMed  Google Scholar 

  • Rodionov DA, Mironov AA, Gelfand MS (2001) Transcriptional regulation of pentose utilisation systems in the Bacillus/Clostridium group of bacteria. FEMS Microbiol Lett 205:305–314

    Article  CAS  PubMed  Google Scholar 

  • Rosen R, Becher D, Buttner K, Biran D, Hecker M, Ron EZ (2004) Highly phosphorylated bacterial proteins. Proteomics 4:3068–3077

    Article  CAS  PubMed  Google Scholar 

  • Schaffer S, Isci N, Zickner B, Durre P (2002) Changes in protein synthesis and identification of proteins specifically induced during solventogenesis in Clostridium acetobutylicum. Electrophoresis 23:110–121

    Article  CAS  PubMed  Google Scholar 

  • Schmidt M, Weuster-Botz D (2012) Reaction engineering studies of acetone–butanol–ethanol fermentation with Clostridium acetobutylicum. Biotechnol J 7:656–661

    Article  CAS  PubMed  Google Scholar 

  • Seeger M, Osorio G, Jerez CA (1996) Phosphorylation of GroEL, DnaK and other proteins from Thiobacillus ferrooxidans grown under different conditions. FEMS Microbiol Lett 138:129–134

    Article  CAS  PubMed  Google Scholar 

  • Servinsky MD, Kiel JT, Dupuy NF, Sund CJ (2010) Transcriptional analysis of differential carbohydrate utilization by Clostridium acetobutylicum. Microbiology 156:3478–3491

    Article  CAS  PubMed  Google Scholar 

  • Sherman M, Goldberg AL (1992) Heat shock in Escherichia coli alters the protein-binding properties of the chaperonin groEL by inducing its phosphorylation. Nature 357:167–169

    Article  CAS  PubMed  Google Scholar 

  • Sherman M, Goldberg AL (1994) Heat shock-induced phosphorylation of GroEL alters its binding and dissociation from unfolded proteins. J Biol Chem 269:31479–31483

    CAS  PubMed  Google Scholar 

  • Sillers R, Al-Hinai MA, Papoutsakis ET (2009) Aldehyde–alcohol dehydrogenase and/or thiolase overexpression coupled with CoA transferase downregulation lead to higher alcohol titers and selectivity in Clostridium acetobutylicum fermentations. Biotechnol Bioeng 102:38–49

    Article  CAS  PubMed  Google Scholar 

  • Speakman HB (1920) Gas production during the acetone and butyl alcohol fermentation of starch. J Biol Chem 43:401–411

    CAS  Google Scholar 

  • Steinhauer K, Jepp T, Hillen W, Stulke J (2002) A novel mode of control of Mycoplasma pneumoniae HPr kinase/phosphatase activity reflects its parasitic lifestyle. Microbiology 148:3277–3284

    CAS  PubMed  Google Scholar 

  • Strader MB, Verberkmoes NC, Tabb DL, Connelly HM, Barton JW, Bruce BD, Pelletier DA, Davison BH, Hettich RL, Larimer FW, Hurst GB (2004) Characterization of the 70S ribosome from Rhodopseudomonas palustris using an integrated “top–down” and “bottom–up” mass spectrometric approach. J Proteome Res 3:965–978

    Article  CAS  PubMed  Google Scholar 

  • Sullivan L, Bennett GN (2006) Proteome analysis and comparison of Clostridium acetobutylicum ATCC 824 and Spo0A strain variants. J Ind Microbiol Biotechnol 33:298–308

    Article  CAS  PubMed  Google Scholar 

  • Tangney M, Galinier A, Deutscher J, Mitchell WJ (2003) Analysis of the elements of catabolite repression in Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biotechnol 6:6–11

    Article  CAS  PubMed  Google Scholar 

  • Tomas CA, Welker NE, Papoutsakis ET (2003) Overexpression of groESL in Clostridium acetobutylicum results in increased solvent production and tolerance, prolonged metabolism, and changes in the cell's transcriptional program. Appl Environ Microbiol 69:4951–4965

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tracy BP (2012) Improving butanol fermentation to enter the advanced biofuel market. mBio 3(6):e00518–12

    Google Scholar 

  • Tummala SB, Junne SG, Papoutsakis ET (2003) Antisense RNA downregulation of coenzyme A transferase combined with alcohol–aldehyde dehydrogenase overexpression leads to predominantly alcohologenic Clostridium acetobutylicum fermentations. J Bacteriol 185:3644–3653

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wiesenborn DP, Rudolph FB, Papoutsakis ET (1989) Coenzyme A transferase from Clostridium acetobutylicum ATCC 824 and its role in the uptake of acids. Appl Environ Microbiol 55:323–329

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yen JY, Nazem-Bokaee H, Freedman BG, Athamneh AI, Senger RS (2013) Deriving metabolic engineering strategies from genome-scale modeling with flux ratio constraints. Biotechnol J 8:581–594

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Tomas CA, Rudolph FB, Papoutsakis ET, Bennett GN (2005) Intracellular butyryl phosphate and acetyl phosphate concentrations in Clostridium acetobutylicum and their implications for solvent formation. Appl Environ Microbiol 71:530–537

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF-2012-C1AAA001-2012M1A2A2026556) through the Technology Development Program to Solve Climate Changes of the Ministry of Education, Science and Technology (MEST) to S.Y. Lee; the Advanced Biomass R&D Center of Korea (2011-0028386) through the Global Frontier Research Program of the MEST to S.Y. Lee; and the Basic Science Research Program (2010-0008826) from the NRF to M.-J. Han. Further support from BioFuelChem and the KAIST EEWS program from the MEST is appreciated.

Conflict of interest

We declare that we do not have conflict of interest.

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Authors and Affiliations

  1. Metabolic and Biomolecular Engineering National Research Laboratory, Department of Chemical and Biomolecular Engineering (BK21 plus program), BioProcess Engineering Research Center, Center for Systems and Synthetic Biotechnology, Institute for the BioCentury, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon, 305-701, South Korea

    Yu-Sin Jang, Joungmin Lee, Jung Ae Im, Yu Hyun Lee & Sang Yup Lee

  2. Department of Biomolecular and Chemical Engineering, Dongyang University, Gyeongbuk, 750-711, South Korea

    Mee-Jung Han

  3. Department of Chemical Engineering and Delaware Biotechnology Institute, University of Delaware, Newark, DE, USA

    Eleftherios Terry Papoutsakis

  4. Department of Biochemistry and Cell Biology, Rice University, Houston, TX, USA

    George Bennett

  5. Bioinformatics Research Center, KAIST, Daejeon, 305-701, South Korea

    Sang Yup Lee

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  1. Yu-Sin Jang
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  2. Mee-Jung Han
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Correspondence to Sang Yup Lee.

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Y.-S. Jang and M.-J. Han contributed equally to this work.

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Jang, YS., Han, MJ., Lee, J. et al. Proteomic analyses of the phase transition from acidogenesis to solventogenesis using solventogenic and non-solventogenic Clostridium acetobutylicum strains. Appl Microbiol Biotechnol 98, 5105–5115 (2014). https://doi.org/10.1007/s00253-014-5738-z

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