Plasmid Effects on Escherichia coli Metabolism

ABSTRACT:  The idea that plasmids replicate within hosts at the expense of cell metabolic energy and preformed cellular blocks depicts plasmids as a kind of molecular parasites that, even when they may eventually provide plasmid-carrying strains with growth advantages over plasmid-free strains, doom hosts to bear an unavoidable metabolic burden. Due to the consistency with experimental data, this idea was rapidly adopted and used as a basis of different hypotheses to explain plasmid-host interactions. In this article we critically discuss current ideas about plasmid effects on host metabolism, and present evidence suggesting that the complex interaction between plasmids and hosts is related to the alteration of the cellular regulatory status.

[1]  Christopher M Thomas Molecular genetics of broad host range plasmid RK2. , 1981, Plasmid.

[2]  K. Low Escherichia coli K-12 F-prime factors, old and new , 1972, Bacteriological reviews.

[3]  H. Lawford,et al.  The relationship between growth enhancement and pet expression in Escherichia coli. , 1996, Applied biochemistry and biotechnology.

[4]  J. H. Slater,et al.  The influence of the growth environment on the stability of a drug resistance plasmid in Escherichia coli K12. , 1979, Journal of general microbiology.

[5]  A. Danchin,et al.  The complete nucleotide sequence of the adenylate cyclase gene of Escherichia coli. , 1984, Nucleic acids research.

[6]  R. Kadner,et al.  Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli. , 1992, Journal of general microbiology.

[7]  J. Tomizawa Control of cole 1 plasmid replication: The process of binding of RNA I to the primer transcript , 1984, Cell.

[8]  J. Adams,et al.  The maintenance of Plasmid-containing organisms in populations of Escherichia coli. , 1981, Journal of general microbiology.

[9]  J. Bailey,et al.  Expression of Vitreoscilla Hemoglobin Is Superior to Horse Heart Myoglobin or Yeast Flavohemoglobin Expression for Enhancing Escherichiacoli Growth in a Microaerobic Bioreactor , 1996, Biotechnology progress.

[10]  G. Edlin,et al.  Expression of tetracycline resistance in pBR322 derivatives reduces the reproductive fitness of plasmid-containing Escherichia coli. , 1985, Gene.

[11]  F. Bolivar,et al.  Plasmids of Escherichia coli as cloning vectors. , 1979, Methods in enzymology.

[12]  Bernd Hitzmann,et al.  In Vivo NMR Analysis of the Influence of Pyruvate Decarboxylase and Alcohol Dehydrogenase of Zymomonas mobilis on the Anaerobic Metabolism of Escherichia coli , 1991 .

[13]  K. Nordström,et al.  Binding between the par region of plasmids R1 and pSC101 and the outer membrane fraction of the host bacteria. , 1983, The EMBO journal.

[14]  J. Messing,et al.  Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. , 1983, Gene.

[15]  G.,et al.  Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli , 2022 .

[16]  B Sonnleitner,et al.  Growth characteristics of Escherichia coli HB101[pGEc47] on defined medium. , 1998, Biotechnology and bioengineering.

[17]  T. Wood,et al.  Depression of protein synthetic capacity due to cloned‐gene expression in E. coli , 1990, Biotechnology and bioengineering.

[18]  Christopher M Thomas,et al.  Active partitioning of bacterial plasmids. , 1992, Journal of general microbiology.

[19]  K. Schügerl,et al.  Gene expression enhancement due to plasmid maintenance , 1995, Journal of bacteriology.

[20]  J. Tomizawa Control of cole1 plasmid replication: Initial interaction of RNA I and the primer transcript is reversible , 1985, Cell.

[21]  R. Skurray,et al.  Stabilization of the cloning vector pACYC184 by insertion of F plasmid leading region sequences. , 1984, Plasmid.

[22]  K. Shanmugam,et al.  Genetic improvement of Escherichia coli for ethanol production: chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II , 1991, Applied and environmental microbiology.

[23]  J. Bailey,et al.  Effect of alteration of the acetic acid synthesis pathway on the fermentation pattern of escherichia coli , 1991, Biotechnology and bioengineering.

[24]  W. Bentley,et al.  Plasmid‐encoded protein: The principal factor in the “metabolic burden” associated with recombinant bacteria , 1990, Biotechnology and bioengineering.

[25]  D. Helinski,et al.  Effect of Growth Conditions on the Formation of the Relaxation Complex of Supercoiled ColE1 Deoxyribonucleic Acid and Protein in Escherichia coli , 1972, Journal of bacteriology.

[26]  B. Dien,et al.  Stabilization of pet operon plasmids and ethanol production in Escherichia coli strains lacking lactate dehydrogenase and pyruvate formate-lyase activities , 1996, Applied and environmental microbiology.

[27]  M. Shimosaka,et al.  Application of hybrid plasmids carrying glycolysis genes to ATP production by Escherichia coli , 1982, Journal of bacteriology.

[28]  J. Bailey,et al.  Expression of Intracellular Hemoglobin Improves Protein Synthesis in Oxygen-Limited Escherichia coli , 1990, Bio/Technology.

[29]  E. Wagner,et al.  Control of phosphoenolpyruvate-dependent phosphotransferase-mediated sugar transport in Escherichia coli by energization of the cell membrane. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[30]  D. Kingsbury,et al.  Stimulation by Cyclic Adenosine Monophosphate of Plasmid Deoxyribonucleic Acid Replication and Catabolite Repression of the Plasmid Deoxyribonucleic Acid-Protein Relaxation Complex , 1973, Journal of bacteriology.

[31]  S. Stirdivant,et al.  Physiological effects of TGFα‐PE40 expression in recombinant Escherichia coli JM109 , 1992 .

[32]  Stanley N Cohen,et al.  Structural and functional analysis of the par region of the pSC101 plasmid , 1984, Cell.

[33]  L. Ingram,et al.  Expression of Different Levels of Ethanologenic Enzymes from Zymomonas mobilis in Recombinant Strains of Escherichia coli , 1988, Applied and environmental microbiology.

[34]  K. Burnstein,et al.  Replication of a low-copy-number plasmid by a plasmid DNA-membrane complex extracted from minicells of Escherichia coli , 1982, Journal of bacteriology.

[35]  S. Benashski,et al.  Interactions of the origin of replication (oriV) and initiation proteins (TrfA) of plasmid RK2 with submembrane domains of Escherichia coli , 1995, Journal of bacteriology.

[36]  W. Dobrogosz,et al.  Stimulation of cytochrome synthesis in Escherichia coli by cyclic AMP. , 1974, Archives of biochemistry and biophysics.

[37]  R. Clowes Molecular structure of bacterial plasmids , 1972, Bacteriological reviews.

[38]  J E Bailey,et al.  Analysis of growth rate effects on productivity of recombinant Escherichia coli populations using molecular mechanism models , 1984, Biotechnology and bioengineering.

[39]  D. Sherratt,et al.  Multimerization of high copy number plasmids causes instability: Cole 1 encodes a determinant essential for plasmid monomerization and stability , 1984, Cell.

[40]  A. Danchin,et al.  Positive regulation of the expression of the Escherichia coli pts operon. Identification of the regulatory regions. , 1992, Journal of molecular biology.

[41]  P. Neubauer,et al.  Impact of plasmid presence and induction on cellular responses in fed batch cultures of Escherichia coli. , 1996, Journal of biotechnology.

[42]  J E Bailey,et al.  Simulations of host–plasmid interactions in Escherichia coli: Copy number, promoter strength, and ribosome binding site strength effects on metabolic activity and plasmid gene expression , 1987, Biotechnology and bioengineering.

[43]  J E Bailey,et al.  Plasmid presence changes the relative levels of many host cell proteins and ribosome components in recombinant Escherichia coli , 1991, Biotechnology and bioengineering.

[44]  G. Stephanopoulos,et al.  Chemostat dynamics of plasmid-bearing, plasmid-free mixed recombinant cultures , 1988 .

[45]  W. Bentley,et al.  A novel structured kinetic modeling approach for the analysis of plasmid instability in recombinant bacterial cultures , 1989, Biotechnology and bioengineering.

[46]  G. Bennett,et al.  Improvement of Biomass Yield and Recombinant Gene Expression in Escherichia coli by Using Fructose as the Primary Carbon Source , 1999, Biotechnology progress.

[47]  N. Nancib,et al.  Variation and modeling of the probability of plasmid loss as a function of growth rate of plasmid‐bearing cells of Escherichia coli during continuous cultures , 1993, Biotechnology and bioengineering.

[48]  W. Firshein,et al.  Plasmid replication and partition in Escherichiacoli: is the cell membrane the key? , 1997, Molecular microbiology.

[49]  K. Nordström,et al.  Mechanisms that contribute to the stable segregation of plasmids. , 1989, Annual review of genetics.

[50]  S. Molin,et al.  Partitioning of plasmid R1 in Escherichia coli. I. Kinetics of loss of plasmid derivatives deleted of the par region. , 1980, Plasmid.

[51]  A. C. Chang,et al.  Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid , 1978, Journal of bacteriology.

[52]  T. Ferenci,et al.  The relationship between external glucose concentration and cAMP levels inside Escherichia coli: implications for models of phosphotransferase-mediated regulation of adenylate cyclase. , 1997, Microbiology.

[53]  M. Saier,et al.  Allosteric regulation of glycerol kinase by enzyme IIIglc of the phosphotransferase system in Escherichia coli and Salmonella typhimurium , 1985, Journal of bacteriology.

[54]  S. Sayadi,et al.  Stability fluctuations of plasmid-bearing cells: immobilization effects. , 1988, Journal of general microbiology.

[55]  J. Bailey,et al.  Heterologous expression of a bacterial haemoglobin improves the growth properties of recombinant Escherichia coli , 1988, Nature.

[56]  Effect of growth rate on plasmid maintenance by Escherichia coli HB101(pAT153). , 1990, Journal of general microbiology.

[57]  C. Branlant,et al.  The EIIGlc Protein Is Involved in Glucose-Mediated Activation of Escherichia coli gapA andgapB-pgk Transcription , 1998, Journal of bacteriology.

[58]  C. Yanisch-Perron,et al.  Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. , 1985, Gene.

[59]  V. Norris,et al.  Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane‐domain formation , 1995, Molecular microbiology.

[60]  W. Konings,et al.  Physical mechanism for regulation of proton solute symport in Escherichia coli. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. R. Brown,et al.  Effect of R plasmid RPI on the nutritional requirements of Escherichia coli in batch culture. , 1979, Journal of general microbiology.

[62]  D J Ayers,et al.  A multiple plasmid-containing Escherichia coli strain: convenient source of size reference plasmid molecules. , 1978, Plasmid.

[63]  A. H. Stouthamer,et al.  Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms. A reevaluation of the method for the determination of ATP production by measuring molar growth yields. , 1973, Biochimica et biophysica acta.

[64]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[65]  U. Stahl,et al.  Replication of plasmids in gram-negative bacteria. , 1989, Microbiological reviews.

[66]  L. Radnedge,et al.  THE DEVELOPMENT OF PLASMID VECTORS , 1999 .

[67]  D. Helinski,et al.  Interactions of plasmid-encoded replication initiation proteins with the origin of DNA replication in the broad host range plasmid RK2. , 1991, The Journal of biological chemistry.

[68]  J. Corchero,et al.  Plasmid maintenance in Escherichia coli recombinant cultures is dramatically, steadily, and specifically influenced by features of the encoded proteins. , 1998, Biotechnology and Bioengineering.

[69]  A. Mcloughlin Plasmid stability and ecological competence in recombinant cultures. , 1994, Biotechnology advances.

[70]  J. Stephenson,et al.  The insertion of large pieces of foreign genetic material reduces the stability of bacterial plasmids. , 1986, Plasmid.

[71]  Manuel Espinosa,et al.  Plasmids Replication and Control of Circular Bacterial , 1998 .

[72]  L. Ingram,et al.  Genetic engineering of ethanol production in Escherichia coli , 1987, Applied and environmental microbiology.

[73]  T. Wood,et al.  Effect of chemically‐induced, cloned‐gene expression on protein synthesis in E. Coli , 1991, Biotechnology and bioengineering.

[74]  G. Bennett,et al.  Effect of modified glucose uptake using genetic engineering techniques on high‐level recombinant protein production in escherichia coli dense cultures , 1994, Biotechnology and bioengineering.

[75]  S. Cohen,et al.  Identification and characterization of recD, a gene affecting plasmid maintenance and recombination in Escherichia coli , 1986, Journal of bacteriology.

[76]  D. Webster,et al.  Variation of oxygen requirement with plasmid size in recombinant Escherichia coli. , 1990, Plasmid.

[77]  D. Helinski,et al.  Suppression of Co1E1 replication properties by the Inc P-1 plasmid RK2 in hybrid plasmids constructed in vitro. , 1979, Journal of molecular biology.

[78]  C. Helmstetter,et al.  Chromosome replication and cell division in plasmid-containing Escherichia coli B/r , 1979, Journal of bacteriology.

[79]  P. Dhurjati,et al.  Effects of dissolved oxygen shock on the stability of recombinant Escherichia coli containing plasmid pKN401 , 1987, Biotechnology and bioengineering.

[80]  J. Bailey,et al.  Influence of expression of the pet operon on intracellular metabolic fluxes of Escherichia coli , 1992, Biotechnology and bioengineering.

[81]  B. Glick Metabolic load and heterologous gene expression. , 1995, Biotechnology advances.

[82]  S. R. Kushner,et al.  Exonucleases I, III, and V are required for stability of ColE1-related plasmids in Escherichia coli , 1984, Journal of bacteriology.

[83]  J E Bailey,et al.  Transcription from plasmid genes, macromolecular stability, and cell‐specific productivity in Escherichia coli carrying copy number mutant plasmids , 1989, Biotechnology and bioengineering.

[84]  J. Lebowitz,et al.  Nucleotide sequence and gene organization of ColE1 DNA. , 1985, The Journal of biological chemistry.

[85]  M. Bidochka,et al.  Bacterial fitness and plasmid loss: the importance of culture conditions and plasmid size. , 1998, Canadian journal of microbiology.

[86]  T. Atlung,et al.  Stability and replication control of Escherichia coli minichromosomes , 1987, Journal of bacteriology.

[87]  J. E. Bouma,et al.  Effects of segregation and selection on instability of plasmid pACYC184 in Escherichia coli B , 1987, Journal of bacteriology.

[88]  J. Bailey,et al.  Comparative Studies of Glucose Catabolism by Escherichia coli Grown in a Complex Medium under Aerobic and Anaerobic Conditions , 1990 .

[89]  C. Sasakawa,et al.  A method of plasmid classification by integrative incompatibility. , 1980, Plasmid.

[90]  A. Peterkofsky,et al.  The Escherichia coli adenylate cyclase complex: activation by phosphoenolpyruvate. , 1978, Journal of supramolecular structure.

[91]  F. Bolivar,et al.  Plasmid vector pBR322 and its special-purpose derivatives--a review. , 1986, Gene.

[92]  J. Bailey,et al.  Studies of Host‐Plasmid Interactions in Recombinant Microorganisms a , 1986, Annals of the New York Academy of Sciences.

[93]  S. J. Parulekar,et al.  Expression of β‐lactamase by recombinant Escherichia coli strains containing plasmids of different sizes—effects of pH, phosphate, and dissolved oxygen , 1989, Biotechnology and bioengineering.

[94]  D. Helinski,et al.  Replication Control and Other Stable Maintenance Mechanisms of Plasmids , 1999 .

[95]  J. Bailey,et al.  Effects of recombinant plasmid content on growth properties and cloned gene product formation in Escherichia coli , 1985, Biotechnology and bioengineering.

[96]  Stanley N Cohen,et al.  Partitioning of bacterial plasmids during cell division: a cis-acting locus that accomplishes stable plasmid inheritance , 1980, Cell.

[97]  A. C. Chang,et al.  Revised Interpretation of the Origin of the pSC101 Plasmid , 1977, Journal of bacteriology.

[98]  J. Bailey,et al.  Theoretical growth yield estimates for recombinant cells. , 1986, Biotechnology and bioengineering.

[99]  J E Bailey,et al.  Flow cytometry analysis of recombinant Saccharomyces cerevisiae populations. , 1986, Cytometry.

[100]  D. Womble,et al.  Genetic and physical map of plasmid NR1: comparison with other IncFII antibiotic resistance plasmids. , 1988, Microbiological reviews.

[101]  W. Weigand,et al.  Effects of recombinant plasmid size on cellular processes in Escherichia coli. , 1987, Plasmid.

[102]  H. P. Charles,et al.  Porphyrin-Accumulating Mutants of Escherichia coli , 1973, Journal of bacteriology.

[103]  G. Lebek,et al.  Generation time-prolonging R plasmids: correlation between increases in the generation time of Escherichia coli caused by R plasmids and their molecular size. , 1980, Plasmid.

[104]  H. Inokuchi,et al.  Cloning and sequencing of a previously unidentified gene that is involved in the biosynthesis of heme in Escherichia coli. , 1995, Gene.

[105]  Cyclic AMP in prokaryotes. , 1992, Microbiological reviews.