Skip to main content

Inducible cell lysis systems in microbial production of bio-based chemicals

Abstract

The release of products from microbial cells is an essential process for industrial scale production of bio-based chemicals. However, traditional methods of cell lysis, e.g., mechanical disruption, chemical solvent extraction, and immobilized enzyme degradation, account for a large share of the total production cost. Thus, an efficient cell lysis system is required to lower the cost. This review has focused on our current knowledge of two cell lysis systems, bacteriophage holin–endolysin system, and lipid enzyme hydrolysis system. These systems are controlled by conditionally inducible regulatory apparatus and applied in microbial production of fatty acids and polyhydroxyalkanoates. Moreover, toxin–antitoxin system is also suggested as alternative for its potential applications in cell lysis. Compared with traditional methods of cell disruption, the inducible cell lysis systems are more economically feasible and easier to control and show a promising perspective in industrial production of bio-based chemicals.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Albertyn J, Hohmann S, Thevelein JM, Prior BA (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14(6):4135–4144

    PubMed  CAS  Google Scholar 

  • Andersson L, Carrière F, Lowe ME, Nilsson Å, Verger R (1996) Pancreatic lipase-related protein 2 but not classical pancreatic lipase hydrolyzes galactolipids. BBA-Lipids Lipid Metab 1302(3):236–240

    Article  Google Scholar 

  • Baneyx F (1999) Recombinant protein expression in Escherichia coli. Curr Opin Biotechnol 10(5):411–421

    PubMed  Article  CAS  Google Scholar 

  • Ben-Amotz A, Avron M (1979) Osmoregulation in the halophilic algae Dunaliella and Asteromonas. Basic Life Sci 14:91–99

    PubMed  CAS  Google Scholar 

  • van den Berg B, Ellis RJ, Dobson CM (1999) Effects of macromolecular crowding on protein folding and aggregation. EMBO J 18(24):6927–6933

    PubMed  Article  Google Scholar 

  • Berry A (1996) Improving production of aromatic compounds in Escherichia coli by metabolic engineering. Trends Biotechnol 14(7):250–256

    PubMed  Article  CAS  Google Scholar 

  • Berry J, Savva C, Holzenburg A, Young R (2010) The lambda spanin components Rz and Rz1 undergo tertiary and quaternary rearrangements upon complex formation. Protein Sci 19(10):1967–1977

    PubMed  Article  CAS  Google Scholar 

  • Berry J, Summer EJ, Struck DK, Young R (2008) The final step in the phage infection cycle: the Rz and Rz1 lysis proteins link the inner and outer membranes. Mol Microbiol 70(2):341–351

    PubMed  Article  CAS  Google Scholar 

  • Biebl H, Marten S, Hippe H, Deckwer W-D (1992) Glycerol conversion to 1, 3-propanediol by newly isolated clostridia. Appl Microbiol Biotechnol 36(5):592–597

    Article  CAS  Google Scholar 

  • Blackburn NT, Clarke AJ (2000) Assay for lytic transglycosylases: a family of peptidoglycan lyases. Anal Biochem 284(2):388–393

    PubMed  Article  CAS  Google Scholar 

  • Buts L, Lah J, Dao-Thi MH, Wyns L, Loris R (2005) Toxin-antitoxin modules as bacterial metabolic stress managers. Trends Biochem Sci 30(12):672–679

    PubMed  Article  CAS  Google Scholar 

  • Chang MP, Bramhall J, Graves S, Bonavida B, Wisnieski B (1989) Internucleosomal DNA cleavage precedes diphtheria toxin-induced cytolysis. Evidence that cell lysis is not a simple consequence of translation inhibition. J Biol Chem 264(26):15261–15267

    PubMed  CAS  Google Scholar 

  • Chen GQ (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38:2434–2446

    PubMed  Article  CAS  Google Scholar 

  • Choonia HS, Lele S (2011) β-Galactosidase release kinetics during ultrasonic disruption of Lactobacillus acidophilus isolated from fermented Eleusine coracana. Food Bioprod Process 89(4):288–293

    Article  CAS  Google Scholar 

  • Díaz E, Munthali M, Lünsdorf H, Höltje JV, Timmis KN (1996) The two-step lysis system of pneumococcal bacteriophage EJ-1 is functional in gram-negative bacteria: triggering of the major pneumococcal autolysin in Escherichia coli. Mol Microbiol 19(4):667–681

    PubMed  Article  Google Scholar 

  • Dahl MK, Schmiedel D, Hillen W (1995) Glucose and glucose-6-phosphate interaction with Xyl repressor proteins from Bacillus spp. may contribute to regulation of xylose utilization. J Bacteriol 177(19):5467–5472

    PubMed  CAS  Google Scholar 

  • Donovan DM, Lardeo M, Foster–Frey J (2006) Lysis of staphylococcal mastitis pathogens by bacteriophage phi11 endolysin. FEMS Microbiol Lett 265(1):133–139

    PubMed  Article  CAS  Google Scholar 

  • Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B, Delattre A-S, Lavigne R (2012) Learning from bacteriophages-advantages and limitations of phage and phage-encoded protein applications. Curr Protein Peptide Sci 13(8):699–722

    Article  CAS  Google Scholar 

  • Elbahloul Y, Steinbuchel A (2009) Large-scale production of poly(3-hydroxyoctanoic acid) by Pseudomonas putida GPo1 and a simplified downstream process. Appl Environ Microbiol 75(3):643–651

    PubMed  Article  CAS  Google Scholar 

  • Feliu J, Cubarsi R, Villaverde A (1998) Optimized release of recombinant proteins by ultrasonication of E. coli cells. Biotechnol Bioeng 58(5):536–540

    PubMed  Article  CAS  Google Scholar 

  • Fell D (1997) Understanding the control of metabolism. Portland Press, Portland

    Google Scholar 

  • Fu CC, Hung TC, Chen JY, Su CH, Wu WT (2010) Hydrolysis of microalgae cell walls for production of reducing sugar and lipid extraction. Bioresour Technol 101(22):8750–8754

    PubMed  Article  CAS  Google Scholar 

  • Grundling A, Blasi U, Young R (2000) Genetic and biochemical analysis of dimer and oligomer interactions of the lambda S holin. J Bacteriol 182(21):6082–6090

    PubMed  Article  CAS  Google Scholar 

  • Gudin C, Thepenier C (1986) Bioconversion of solar energy into organic chemicals by microalgae. Adv Biotechnol Process 6:73–100

    CAS  Google Scholar 

  • Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14):4121–4130

    PubMed  CAS  Google Scholar 

  • Hamilton W, Sale A (1967) Effects of high electric fields on microorganisms: II Mechanism of action of the lethal effect. BBA-Gen Subjects 148(3):789–800

    Article  CAS  Google Scholar 

  • Hayes F (2003) Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301(5639):1496–1499

    PubMed  Article  CAS  Google Scholar 

  • Helmsing P (1969) Purification and properties of galactolipase. BBA-Enzymol 178(3):519–533

    Article  CAS  Google Scholar 

  • Henrich B, Lubitz W, Plapp R (1982) Lysis of Escherichia coli by induction of cloned ΦX174 genes. Mol Gen Genet 185(3):493–497

    PubMed  Article  CAS  Google Scholar 

  • Ho CW, Chew TK, Ling TC, Kamaruddin S, Tan WS, Tey BT (2006) Efficient mechanical cell disruption of Escherichia coli by an ultrasonicator and recovery of intracellular hepatitis B core antigen. Process Biochem 41(8):1829–1834

    Article  CAS  Google Scholar 

  • Hori K, Kaneko M, Tanji Y, Xing XH, Unno H (2002) Construction of self-disruptive Bacillus megaterium in response to substrate exhaustion for polyhydroxybutyrate production. Appl Microbiol Biotechnol 59(2–3):211–216

    PubMed  CAS  Google Scholar 

  • Iida Y, Tuziuti T, Yasui K, Kozuka T, Towata A (2008) Protein release from yeast cells as an evaluation method of physical effects in ultrasonic field. Ultrason Sonochem 15(6):995–1000

    PubMed  Article  CAS  Google Scholar 

  • Ikeda M, Katsumata R (1999) Hyperproduction of tryptophan by Corynebacterium glutamicum with the modified pentose phosphate pathway. Appl Environ Microbiol 65(6):2497–2502

    PubMed  CAS  Google Scholar 

  • Ito H, Sato K, Enei H, Hirose Y (1990) Improvement in microbial production of L-tyrosine by gene dosage effect of aroL gene encoding shikimate kinase. Agric Biol Chem 54(3):823–824

    PubMed  Article  CAS  Google Scholar 

  • Kohler GA, Brenot A, Haas-Stapleton E, Agabian N, Deva R, Nigam S (2006) Phospholipase A2 and phospholipase B activities in fungi. BBA-Mol Cell Biol 1761(11):1391–1399

    Google Scholar 

  • López-Maury L, García-Domínguez M, Florencio FJ, Reyes JC (2002) A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803. Mol Microbiol 43(1):247–256

    PubMed  Article  Google Scholar 

  • Lim JA, Shin H, Kang DH, Ryu S (2012) Characterization of endolysin from a Salmonella Typhimurium-infecting bacteriophage SPN1S. Res Microbiol 163(3):233–241

    PubMed  Article  CAS  Google Scholar 

  • Liu H, Yu C, Feng D, Cheng T, Meng X, Liu W, Zou H, Xian M (2012) Production of extracellular fatty acid using engineered Escherichia coli. Microb Cell Fact 11(1):41–54

    PubMed  Article  Google Scholar 

  • Liu X, Curtiss R III (2009) Nickel-inducible lysis system in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA 106(51):21550–21554

    PubMed  Article  CAS  Google Scholar 

  • Liu X, Curtiss R III (2012) Thermorecovery of cyanobacterial fatty acids at elevated temperatures. J Biotechnol 161(4):445–449

    PubMed  Article  CAS  Google Scholar 

  • Liu X, Fallon S, Sheng J, Curtiss R III (2011a) CO2-limitation-inducible green recovery of fatty acids from cyanobacterial biomass. Proc Natl Acad Sci USA 108(17):6905–6908

    PubMed  Article  CAS  Google Scholar 

  • Liu X, Sheng J, Curtiss R III (2011b) Fatty acid production in genetically modified cyanobacteria. Proc Natl Acad Sci USA 108(17):6899–6904

    PubMed  Article  CAS  Google Scholar 

  • Loessner MJ (2005) Bacteriophage endolysins-current state of research and applications. Curr Opin Microbiol 8(4):480–487

    PubMed  Article  CAS  Google Scholar 

  • Low LY, Yang C, Perego M, Osterman A, Liddington RC (2005) Structure and lytic activity of a Bacillus anthracis prophage endolysin. J Biol Chem 280(42):35433–35439

    PubMed  Article  CAS  Google Scholar 

  • Lubitz W, Schmid R, Plapp R (1981) Alterations of the cytoplasmic and outer membranes of Escherichia coli infected with bacteriophage ϕX174. Curr Microbiol 5(1):45–50

    Article  CAS  Google Scholar 

  • Martinez V, Garcia P, Garcia JL, Prieto MA (2011) Controlled autolysis facilitates the polyhydroxyalkanoate recovery in Pseudomonas putida KT2440. Microb Biotechnol 4(4):533–547

    PubMed  Article  CAS  Google Scholar 

  • McGinn PJ, Price GD, Maleszka R, Badger MR (2003) Inorganic carbon limitation and light control the expression of transcripts related to the CO2-concentrating mechanism in the cyanobacterium Synechocystis sp. strain PCC6803. Plant Physiol 132(1):218–229

    PubMed  Article  CAS  Google Scholar 

  • McMillan JR, Watson IA, Ali M, Jaafar W (2013) Evaluation and comparison of algal cell disruption methods: microwave, waterbath, blender, ultrasonic and laser treatment. Appl Energy 103:128–134

    Article  Google Scholar 

  • van Melderen L, Thi MHD, Lecchi P, Gottesman S, Couturier M, Maurizi MR (1996) ATP-dependent degradation of CcdA by Lon protease. J Biol Chem 271(44):27730–27738

    PubMed  Article  Google Scholar 

  • Mendes-Pinto M, Raposo M, Bowen J, Young A, Morais R (2001) Evaluation of different cell disruption processes on encysted cells of Haematococcus pluvialis: effects on astaxanthin recovery and implications for bio-availability. J Appl Phycol 13(1):19–24

    Article  Google Scholar 

  • Millard CS, Chao Y-P, Liao JC, Donnelly MI (1996) Enhanced production of succinic acid by overexpression of phosphoenolpyruvate carboxylase in Escherichia coli. Appl Environ Microbiol 62(5):1808–1810

    PubMed  CAS  Google Scholar 

  • Molina Grima E, Belarbi EH, Acien Fernandez F, Robles Medina A, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20(7–8):491–515

    PubMed  Article  CAS  Google Scholar 

  • Moniruzzaman M, Ingram LO (1998) Ethanol production from dilute acid hydrolysate of rice hulls using genetically engineered Escherichia coli. Biotechnol Lett 20(10):943–947

    Article  CAS  Google Scholar 

  • Numanoğlu Y, Sungur S (2004) β-Galactosidase from Kluyveromyces lactis cell disruption and enzyme immobilization using a cellulose-gelatin carrier system. Process Biochem 39(6):705–711

    Article  Google Scholar 

  • Peralta-Yahya PP, Keasling JD (2010) Advanced biofuel production in microbes. J Biotechnol 5(2):147–162

    Article  CAS  Google Scholar 

  • Ramsay J, Berger E, Voyer R, Chavarie C, Ramsay B (1994) Extraction of poly-3-hydroxybutyrate using chlorinated solvents. Biotechnol Tech 8(8):589–594

    Article  CAS  Google Scholar 

  • Rapp P (1995) Production, regulation, and some properties of lipase activity from Fusarium oxysporum f. sp. vasinfectum. Enzyme Microb Technol 17(9):832–838

    Article  CAS  Google Scholar 

  • Rathi DN, Amir HG, Abed RM, Kosugi A, Arai T, Sulaiman O, Hashim R, Sudesh K (2013) Polyhydroxyalkanoate biosynthesis and simplified polymer recovery by a novel moderately halophilic bacterium isolated from hypersaline microbial mats. J Appl Microbiol 114(2):384–395

    PubMed  Article  CAS  Google Scholar 

  • Resch S, Gruber K, Wanner G, Slater S, Dennis D, Lubitz W (1998) Aqueous release and purification of poly(β-hydroxybutyrate) from Escherichia coli. J Biotechnol 65(2):173–182

    PubMed  Article  CAS  Google Scholar 

  • Roof WD, Young R (1993) ϕX174 E complements λ S and R dysfunction for host cell lysis. J Bacteriol 175(12):3909–3912

    PubMed  CAS  Google Scholar 

  • Rosenstein R, Gotz F (2000) Staphylococcal lipases: biochemical and molecular characterization. Biochimie 82(11):1005–1014

    PubMed  Article  CAS  Google Scholar 

  • de Ruyter P, Kuipers OP, Meijer WC, de Vos WM (1997) Food-grade controlled lysis of Lactococcus lactis for accelerated cheese ripening. Nat Biotechnol 15(10):976–979

    PubMed  Article  Google Scholar 

  • Rygus T, Scheler A, Allmansberger R, Hillen W (1991) Molecular cloning, structure, promoters and regulatory elements for transcription of the Bacillus megaterium encoded regulon for xylose utilization. Arch Microbiol 155(6):535–542

    PubMed  Article  CAS  Google Scholar 

  • São-José C, Nascimento J, Parreira R, Santos MA, Macgrath S, van Sinderen D (2007) Release of progeny phages from infected cells. In: McGrath S, van Sinderen D (eds) Bacteriophages: Genetics and Molecular Biology. Caister Academic Press, Norfolk, pp 309–334

    Google Scholar 

  • Sanders JW, Venema G, Kok J (1997) A chloride-inducible gene expression cassette and its use in induced lysis of Lactococcus lactis. Appl Environ Microbiol 63(12):4877–4882

    PubMed  CAS  Google Scholar 

  • Sandvig K, van Deurs B (1992) Toxin-induced cell lysis: protection by 3-methyladenine and cycloheximide. Exp Cell Res 200(2):253–262

    PubMed  Article  CAS  Google Scholar 

  • Savva CG, Dewey JS, Deaton J, White RL, Struck DK, Holzenburg A, Young R (2008) The holin of bacteriophage lambda forms rings with large diameter. Mol Microbiol 69(4):784–793

    PubMed  Article  CAS  Google Scholar 

  • Sheng J, Vannela R, Rittmann BE (2011) Evaluation of cell-disruption effects of pulsed-electric-field treatment of Synechocystis PCC 6803. Environ Sci Technol 45(8):3795–3802

    PubMed  Article  CAS  Google Scholar 

  • Short FL, Blower TR, Salmond GPC (2012) A promiscuous antitoxin of bacteriophage T4 ensures successful viral replication. Mol Microbiol 83(4):665–668

    PubMed  Article  CAS  Google Scholar 

  • Skerra A (1994) Use of the tetracycline promoter for the tightly regulated production of a murine antibody fragment in Escherichia coli. Gene 151(1–2):131–135

    PubMed  Article  CAS  Google Scholar 

  • Steinbüchel A, Müller M (1986) Glycerol, a metabolic end product of Trichomonas vaginalis and Tritrichomonas foetus. Mol Biochem Parasitol 20(1):45–55

    PubMed  Article  Google Scholar 

  • Tsujimoto Y, Shimizu S (2007) Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12(5):835–840

    PubMed  Article  CAS  Google Scholar 

  • Wang IN, Deaton J, Young R (2003) Sizing the holin lesion with an endolysin-β-galactosidase fusion. J Bacteriol 185(3):779–787

    PubMed  Article  CAS  Google Scholar 

  • Weaver JC, Chizmadzhev YA (1996) Theory of electroporation: a review. Bioelectrochem Bioenerg 41(2):135–160

    Article  CAS  Google Scholar 

  • Wirtz E, Leal S, Ochatt C, Cross GAM (1999) A tightly regulated inducible expression system for conditional gene knock-outs and dominant-negative genetics in Trypanosoma brucei. Mol Biochem Parasitol 99(1):89–101

    PubMed  Article  CAS  Google Scholar 

  • Witte A, Blasi U, Halfmann G, Szostak M, Wanner G, Lubitz W (1990) PhiX174 protein E-mediated lysis of Escherichia coli. Biochimie 72(2–3):191–200

    PubMed  Article  CAS  Google Scholar 

  • Witte A, Lubitz W (1989) Biochemical characterization of PhiX174-protein-E-mediated lysis of Escherichia coli. Eur J Biochem 180(2):393–398

    PubMed  Article  CAS  Google Scholar 

  • Young R (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56(3):430–481

    PubMed  CAS  Google Scholar 

  • Young R (2002) Bacteriophage holins: deadly diversity. J Mol Microbiol Biotechnol 4(1):21–36

    PubMed  CAS  Google Scholar 

  • Yu H, Shi Y, Sun X, Luo H, Shen Z (2003) Effect of poly(β-hydroxybutyrate) accumulation on the stability of a recombinant plasmid in Escherichia coli. J Biosci Bioeng 96(2):179–183

    PubMed  CAS  Google Scholar 

  • Yu H, Yin J, Li H, Yang S, Shen Z (2000) Construction and selection of the novel recombinant Escherichia coli strain for poly(β-hydroxybutyrate) production. J Biosci Bioeng 89(4):307–311

    PubMed  Article  CAS  Google Scholar 

  • Yu S, Yu S, Han W, Wang H, Zheng B, Feng Y (2010) A novel thermophilic lipase from Fervidobacterium nodosum Rt17-B1 representing a new subfamily of bacterial lipases. J Mol Catal B-Enzym 66(1–2):81–89

    Article  CAS  Google Scholar 

  • Zeikus J (1980) Chemical and fuel production by anaerobic bacteria. Annu Rev Microbiol 34(1):423–464

    PubMed  Article  CAS  Google Scholar 

  • Zhang X, Pan Z, Fang Q, Zheng J, Hu M, Jiao X (2009) An auto-inducible Escherichia coli lysis system controlled by magnesium. J Microbiol Methods 79(2):199–204

    PubMed  Article  CAS  Google Scholar 

  • Zhang Z, Blewett J, Thomas C (1999) Modelling the effect of osmolality on the bursting strength of yeast cells. J Biotechnol 71(1):17–24

    PubMed  Article  CAS  Google Scholar 

  • Zheng H, Yin J, Gao Z, Huang H, Ji X, Dou C (2011) Disruption of Chlorella vulgaris cells for the release of biodiesel-producing lipids: a comparison of grinding, ultrasonication, bead milling, enzymatic lysis, and microwaves. Appl Biochem Biotechnol 164(7):1215–1224

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgment

This research was financially supported by 100-Talent Project of CAS (for GZ), Director Innovation Foundation of QIBEBT, CAS (Y112141105), National Natural Scientific Foundation of China (31200030), National Science and Technology Program (2012BAD32B06), and National 863 Project of China (SS2013AA050703-2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guang Zhao.

Additional information

Yongqiang Gao and Xinjun Feng contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gao, Y., Feng, X., Xian, M. et al. Inducible cell lysis systems in microbial production of bio-based chemicals. Appl Microbiol Biotechnol 97, 7121–7129 (2013). https://doi.org/10.1007/s00253-013-5100-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-5100-x

Keywords

  • Cell lysis systems
  • Inducible regulatory apparatus
  • Holin–endolysin system
  • Lipid enzyme system
  • Toxin–antitoxin system