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References
Contents
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[1]J. T. Trevors and M. H. Saier, Jr.: Thermodynamic perspectives on genetic instructions, the laws of biology and diseased states. C R Biol, 334(1), 1-5 (2011)
[2]M. DeLisi and M. G. Vaughn: The Vindication of Lamarck? Epigenetics at the Intersection of Law and Mental Health. Behav Sci Law, 33(5), 607-28 (2015)
[3]A. Galera: The Impact of Lamarck’s Theory of Evolution Before Darwin’s Theory. J Hist Biol (2016) doi:10.1.007/s10739-015-9432-5
[4]M. K. Skinner: Environmental Epigenetics and a Unified Theory of the Molecular Aspects of Evolution: A Neo-Lamarckian Concept that Facilitates Neo-Darwinian Evolution. Genome Biol Evol, 7(5), 1296-302 (2015)
[5]W. W. Burggren: Epigenetics as a source of variation in comparative animal physiology - or - Lamarck is lookin’ pretty good these days. J Exp Biol, 217(Pt 5), 682-9 (2014)
[6]J. Cairns, J. Overbaugh and S. Miller: The origin of mutants. Nature, 335(6186), 142-5 (1988) doi:10.1.038/335142a0
[7]B. G. Hall: Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics, 126(1), 5-16 (1990)
[8]P. L. Foster and J. Cairns: Mechanisms of directed mutation. Genetics, 131(4), 783-9 (1992)
[9]J. R. Roth, E. Kugelberg, A. B. Reams, E. Kofoid and D. I. Andersson: Origin of mutations under selection: the adaptive mutation controversy. Annu Rev Microbiol, 60, 477-501 (2006)
[10]I. Abubakar, R. Welfare, J. Moore and J. M. Watson: Surveillance of air-travel-related tuberculosis incidents, England and Wales: 2007-2008. Euro Surveill, 13(23) (2008)
[11]A. B. Reams and J. R. Roth: Mechanisms of gene duplication and amplification. Cold Spring Harb Perspect Biol, 7(2), a016592 (2015)
[12]Z. Zhang and M. H. Saier, Jr.: A mechanism of transposon-mediated directed mutation. Mol Microbiol, 74(1), 29-43 (2009)
[13]Z. Zhang and M. H. Saier, Jr.: A novel mechanism of transposon-mediated gene activation. PLoS Genet, 5(10), e1000689 (2009)
[14]M. K. Burke: How does adaptation sweep through the genome? Insights from long-term selection experiments. Proc Biol Sci, 279(1749), 5029-38 (2012)
[15]L. H. Caporale and J. Doyle: In Darwinian evolution, feedback from natural selection leads to biased mutations. Ann N Y Acad Sci, 1305, 18-28 (2013)
[16]C. B. Mc: The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A, 36(6), 344-55 (1950)
[17]N. C. Comfort: From controlling elements to transposons: Barbara McClintock and the Nobel Prize. Trends Genet, 17(8), 475-8 (2001)
[18]C. R. Huang, K. H. Burns and J. D. Boeke: Active transposition in genomes. Annu Rev Genet, 46, 651-75 (2012)
[19]D. De Palmenaer, P. Siguier and J. Mahillon: IS4 family goes genomic. BMC Evol Biol, 8, 18 (2008)
[20]P. Siguier, E. Gourbeyre and M. Chandler: Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev, 38(5), 865-91 (2014)
[21]E. V. Koonin, M. Krupovic and N. Yutin: Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Ann N Y Acad Sci, 1341, 10-24 (2015)
[22]J. Z. Jacobs, J. D. Rosado-Lugo, S. Cranz-Mileva, K. M. Ciccaglione, V. Tournier and M. Zaratiegui: Arrested replication forks guide retrotransposon integration. Science, 349(6255), 1549-53 (2015)
[23]B. Swingle, M. O’Carroll, D. Haniford and K. M. Derbyshire: The effect of host-encoded nucleoid proteins on transposition: H-NS influences targeting of both IS903 and Tn10. Mol Microbiol, 52(4), 1055-67 (2004)
[24]E. C. Lin: Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol, 30, 535-78 (1976)
[25]G. Sweet, C. Gandor, R. Voegele, N. Wittekindt, J. Beuerle, V. Truniger, E. C. Lin and W. Boos: Glycerol facilitator of Escherichia coli: cloning of glpF and identification of the glpF product. J Bacteriol, 172(1), 424-30 (1990)
[26]C. Mao, Z. Ozer, M. Zhou and F. M. Uckun: X-Ray structure of glycerol kinase complexed with an ATP analog implies a novel mechanism for the ATP-dependent glycerol phosphorylation by glycerol kinase. Biochem Biophys Res Commun, 259(3), 640-4 (1999)
[27]A. D. Fraser and H. Yamazaki: Characterization of an Escherichia coli mutant which utilizes glycerol in the absence of cyclic adenosine monophosphate. Can J Microbiol, 26(3), 393-6 (1980)
[28]J. R. Lupski, Y. H. Zhang, M. Rieger, M. Minter, B. Hsu, B. G. Ooi, T. Koeuth and E. R. McCabe: Mutational analysis of the Escherichia coli glpFK region with Tn5 mutagenesis and the polymerase chain reaction. J Bacteriol, 172(10), 6129-34 (1990)
[29]D. L. Weissenborn, N. Wittekindt and T. J. Larson: Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J Biol Chem, 267(9), 6122-31 (1992)
[30]G. Zeng, S. Ye and T. J. Larson: Repressor for the sn-glycerol 3-phosphate regulon of Escherichia coli K-12: primary structure and identification of the DNA-binding domain. J Bacteriol, 178(24), 7080-9 (1996)
[31]J. Green, M. R. Stapleton, L. J. Smith, P. J. Artymiuk, C. Kahramanoglou, D. M. Hunt and R. S. Buxton: Cyclic-AMP and bacterial cyclic-AMP receptor proteins revisited: adaptation for different ecological niches. Curr Opin Microbiol, 18, 1-7 (2014)
[32]A. Cournac and J. Plumbridge: DNA looping in prokaryotes: experimental and theoretical approaches. J Bacteriol, 195(6), 1109-19 (2013)
[33]M. H. Saier, Jr.: Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev, 53(1), 109-20 (1989)
[34]A. Vastermark and M. H. Saier, Jr.: The involvement of transport proteins in transcriptional and metabolic regulation. Curr Opin Microbiol, 18, 8-15 (2014)
[35]Z. Zhang and M. H. Saier, Jr.: Transposon-mediated activation of the Escherichia coli glpFK operon is inhibited by specific DNA-binding proteins: Implications for stress-induced transposition events. Mutat Res, 793-794, 22-31 (2016)
[36]F. Heppner and J. R. Mose: (Oncolysis of malignant gliomas through apathogenic clostridia (strain “M 55”)). Zentralbl Neurochir, 27(4), 183-92 (1966)
[37]M. H. Saier, Jr., S. Chauvaux, G. M. Cook, J. Deutscher, I. T. Paulsen, J. Reizer and J. J. Ye: Catabolite repression and inducer control in Gram-positive bacteria. Microbiology, 142 ( Pt 2), 217-30 (1996)
[38]M. H. Saier, Jr. and C. E. Ballou: The 6-O-methylglucose-containing lipopolysaccharide of Mycobacterium phlei. Identification of D-glyceric acid and 3-O-methyl-D-glucose in the polysaccharide. J Biol Chem, 243(5), 992-1005 (1968)
[39]X. M. He and H. W. Liu: Formation of unusual sugars: mechanistic studies and biosynthetic applications. Annu Rev Biochem, 71, 701-54 (2002)
[40]C. Kumar, K. Yadav, G. Archana and G. Naresh Kumar: 2-ketogluconic acid secretion by incorporation of Pseudomonas putida KT 2440 gluconate dehydrogenase (gad) operon in Enterobacter asburiae PSI3 improves mineral phosphate solubilization. Curr Microbiol, 67(3), 388-94 (2013) d
[41]B. L. Moller: Functional diversifications of cyanogenic glucosides. Curr Opin Plant Biol, 13(3), 338-47 (2010)
[42]F. M. Xi, C. T. Li, J. L. Mi, Z. J. Wu and W. S. Chen: Three new olean-type triterpenoid saponins from aerial parts of Eclipta prostrata (L.). Nat Prod Res, 28(1), 35-40 (2014)
[43]Z. Zhang, M. R. Yen and M. H. Saier, Jr.: Precise excision of IS5 from the intergenic region between the fucPIK and the fucAO operons and mutational control of fucPIK operon expression in Escherichia coli. J Bacteriol, 192(7), 2013-9 (2010)
[44]C. K. Holtman, A. C. Pawlyk, N. Meadow, S. Roseman and D. W. Pettigrew: IIA(Glc) allosteric control of Escherichia coli glycerol kinase: binding site cooperative transitions and cation-promoted association by Zinc(II). Biochemistry, 40(47), 14302-8 (2001)
[45]B. U. Feucht and M. H. Saier, Jr.: Fine control of adenylate cyclase by the phosphoenolpyruvate:sugar phosphotransferase systems in Escherichia coli and Salmonella typhimurium. J Bacteriol, 141(2), 603-10 (1980)
[46]M. H. Saier, Jr.: The bacterial chromosome. Crit Rev Biochem Mol Biol, 43(2), 89-134 (2008)
[47]M. S. Wright, A. Iovleva, M. R. Jacobs, R. A. Bonomo and M. D. Adams: Genome dynamics of multidrug-resistant Acinetobacter baumannii during infection and treatment. Genome Med, 8(1), 26 (2016)
[48]X. Wang and T. K. Wood: IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way. ISME J, 5(9), 1517-25 (2011)
[49]M. Kricker and B. G. Hall: Directed evolution of cellobiose utilization in Escherichia coli K12. Mol Biol Evol, 1(2), 171-82 (1984)
[50]B. G. Hall: On alternatives to selection-induced mutation in the Bgl operon of Escherichia coli. Mol Biol Evol, 11(2), 159-68 (1994)
[51]B. G. Hall: On the specificity of adaptive mutations. Genetics, 145(1), 39-44 (1997)
[52]B. G. Hall: Transposable elements as activators of cryptic genes in E. coli. Genetica, 107(1-3), 181-7 (1999)
[53]J. Vandecraen, P. Monsieurs, M. Mergeay, N. Leys, A. Aertsen and R. Van Houdt: Zinc-Induced Transposition of Insertion Sequence Elements Contributes to Increased Adaptability of Cupriavidus metallidurans. Front Microbiol, 7, 359 (2016)
[54]T. T. Tseng, K. S. Gratwick, J. Kollman, D. Park, D. H. Nies, A. Goffeau and M. H. Saier, Jr.: The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol, 1(1), 107-25 (1999)
[55]R. A. Elbarbary, B. A. Lucas and L. E. Maquat: Retrotransposons as regulators of gene expression. Science, 351(6274), aac7247 (2016)
[56]R. A. Watson and E. Szathmary: How Can Evolution Learn? Trends Ecol Evol, 31(2), 147-57 (2016)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
1 Department of Molecular Biology, Division of Biological Sciences, University of California at San Diego, La Jolla, CA 92093-0116, USA
Abstract
Transposon-mediated “directed” mutations occur at higher frequencies when beneficial than when detrimental and relieve the stress that causes them. The first and best-studied example involves regulation of Insertion Sequence-5 (IS5) insertion into a specific activating site upstream of the glycerol utilization operon in Escherichia coli, glpFK. This event promotes high level expression of the glpFK operon, allowing glycerol utilization in wild type cells under inhibitory conditions. The phosphoenolpyruvate-dependent, sugar transporting, phosphotransferase system (PTS) influences this process by regulating cytoplasmic glycerol-3-phosphate and cyclic AMP concentrations. Insertion frequencies are determined by IS5-specific tetranucleotide target sequences in stress-induced (DNA) duplex destabilization (SIDD) structures counteracted by two DNA binding proteins, GlpR and Crp which directly inhibit insertion, responding to cytoplasmic glycerol-3-phosphate and cyclic AMP, respectively. Expression of the E. coli master regulator of flagellar gene control, flhDC, is subject to activation by IS elements by a directed mechanism, and zinc-induced transposon-mediated zinc resistance has been demonstrated in Cupriavidus metallidurans. The use of DNA conformation and DNA binding proteins to control transposon hopping also occurs in eukaryotes.
Keywords
- Adaptive Mutation
- Directed Mutation
- Transposons
- Insertion Sequence Elements
- DNA Binding Proteins
- Evolution
- Review
References
- [1] J. T. Trevors and M. H. Saier, Jr.: Thermodynamic perspectives on genetic instructions, the laws of biology and diseased states. C R Biol, 334(1), 1-5 (2011)
- [2] M. DeLisi and M. G. Vaughn: The Vindication of Lamarck? Epigenetics at the Intersection of Law and Mental Health. Behav Sci Law, 33(5), 607-28 (2015)
- [3] A. Galera: The Impact of Lamarck’s Theory of Evolution Before Darwin’s Theory. J Hist Biol (2016) doi:10.1.007/s10739-015-9432-5
- [4] M. K. Skinner: Environmental Epigenetics and a Unified Theory of the Molecular Aspects of Evolution: A Neo-Lamarckian Concept that Facilitates Neo-Darwinian Evolution. Genome Biol Evol, 7(5), 1296-302 (2015)
- [5] W. W. Burggren: Epigenetics as a source of variation in comparative animal physiology - or - Lamarck is lookin’ pretty good these days. J Exp Biol, 217(Pt 5), 682-9 (2014)
- [6] J. Cairns, J. Overbaugh and S. Miller: The origin of mutants. Nature, 335(6186), 142-5 (1988) doi:10.1.038/335142a0
- [7] B. G. Hall: Spontaneous point mutations that occur more often when advantageous than when neutral. Genetics, 126(1), 5-16 (1990)
- [8] P. L. Foster and J. Cairns: Mechanisms of directed mutation. Genetics, 131(4), 783-9 (1992)
- [9] J. R. Roth, E. Kugelberg, A. B. Reams, E. Kofoid and D. I. Andersson: Origin of mutations under selection: the adaptive mutation controversy. Annu Rev Microbiol, 60, 477-501 (2006)
- [10] I. Abubakar, R. Welfare, J. Moore and J. M. Watson: Surveillance of air-travel-related tuberculosis incidents, England and Wales: 2007-2008. Euro Surveill, 13(23) (2008)
- [11] A. B. Reams and J. R. Roth: Mechanisms of gene duplication and amplification. Cold Spring Harb Perspect Biol, 7(2), a016592 (2015)
- [12] Z. Zhang and M. H. Saier, Jr.: A mechanism of transposon-mediated directed mutation. Mol Microbiol, 74(1), 29-43 (2009)
- [13] Z. Zhang and M. H. Saier, Jr.: A novel mechanism of transposon-mediated gene activation. PLoS Genet, 5(10), e1000689 (2009)
- [14] M. K. Burke: How does adaptation sweep through the genome? Insights from long-term selection experiments. Proc Biol Sci, 279(1749), 5029-38 (2012)
- [15] L. H. Caporale and J. Doyle: In Darwinian evolution, feedback from natural selection leads to biased mutations. Ann N Y Acad Sci, 1305, 18-28 (2013)
- [16] C. B. Mc: The origin and behavior of mutable loci in maize. Proc Natl Acad Sci U S A, 36(6), 344-55 (1950)
- [17] N. C. Comfort: From controlling elements to transposons: Barbara McClintock and the Nobel Prize. Trends Genet, 17(8), 475-8 (2001)
- [18] C. R. Huang, K. H. Burns and J. D. Boeke: Active transposition in genomes. Annu Rev Genet, 46, 651-75 (2012)
- [19] D. De Palmenaer, P. Siguier and J. Mahillon: IS4 family goes genomic. BMC Evol Biol, 8, 18 (2008)
- [20] P. Siguier, E. Gourbeyre and M. Chandler: Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev, 38(5), 865-91 (2014)
- [21] E. V. Koonin, M. Krupovic and N. Yutin: Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Ann N Y Acad Sci, 1341, 10-24 (2015)
- [22] J. Z. Jacobs, J. D. Rosado-Lugo, S. Cranz-Mileva, K. M. Ciccaglione, V. Tournier and M. Zaratiegui: Arrested replication forks guide retrotransposon integration. Science, 349(6255), 1549-53 (2015)
- [23] B. Swingle, M. O’Carroll, D. Haniford and K. M. Derbyshire: The effect of host-encoded nucleoid proteins on transposition: H-NS influences targeting of both IS903 and Tn10. Mol Microbiol, 52(4), 1055-67 (2004)
- [24] E. C. Lin: Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol, 30, 535-78 (1976)
- [25] G. Sweet, C. Gandor, R. Voegele, N. Wittekindt, J. Beuerle, V. Truniger, E. C. Lin and W. Boos: Glycerol facilitator of Escherichia coli: cloning of glpF and identification of the glpF product. J Bacteriol, 172(1), 424-30 (1990)
- [26] C. Mao, Z. Ozer, M. Zhou and F. M. Uckun: X-Ray structure of glycerol kinase complexed with an ATP analog implies a novel mechanism for the ATP-dependent glycerol phosphorylation by glycerol kinase. Biochem Biophys Res Commun, 259(3), 640-4 (1999)
- [27] A. D. Fraser and H. Yamazaki: Characterization of an Escherichia coli mutant which utilizes glycerol in the absence of cyclic adenosine monophosphate. Can J Microbiol, 26(3), 393-6 (1980)
- [28] J. R. Lupski, Y. H. Zhang, M. Rieger, M. Minter, B. Hsu, B. G. Ooi, T. Koeuth and E. R. McCabe: Mutational analysis of the Escherichia coli glpFK region with Tn5 mutagenesis and the polymerase chain reaction. J Bacteriol, 172(10), 6129-34 (1990)
- [29] D. L. Weissenborn, N. Wittekindt and T. J. Larson: Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J Biol Chem, 267(9), 6122-31 (1992)
- [30] G. Zeng, S. Ye and T. J. Larson: Repressor for the sn-glycerol 3-phosphate regulon of Escherichia coli K-12: primary structure and identification of the DNA-binding domain. J Bacteriol, 178(24), 7080-9 (1996)
- [31] J. Green, M. R. Stapleton, L. J. Smith, P. J. Artymiuk, C. Kahramanoglou, D. M. Hunt and R. S. Buxton: Cyclic-AMP and bacterial cyclic-AMP receptor proteins revisited: adaptation for different ecological niches. Curr Opin Microbiol, 18, 1-7 (2014)
- [32] A. Cournac and J. Plumbridge: DNA looping in prokaryotes: experimental and theoretical approaches. J Bacteriol, 195(6), 1109-19 (2013)
- [33] M. H. Saier, Jr.: Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev, 53(1), 109-20 (1989)
- [34] A. Vastermark and M. H. Saier, Jr.: The involvement of transport proteins in transcriptional and metabolic regulation. Curr Opin Microbiol, 18, 8-15 (2014)
- [35] Z. Zhang and M. H. Saier, Jr.: Transposon-mediated activation of the Escherichia coli glpFK operon is inhibited by specific DNA-binding proteins: Implications for stress-induced transposition events. Mutat Res, 793-794, 22-31 (2016)
- [36] F. Heppner and J. R. Mose: (Oncolysis of malignant gliomas through apathogenic clostridia (strain “M 55”)). Zentralbl Neurochir, 27(4), 183-92 (1966)
- [37] M. H. Saier, Jr., S. Chauvaux, G. M. Cook, J. Deutscher, I. T. Paulsen, J. Reizer and J. J. Ye: Catabolite repression and inducer control in Gram-positive bacteria. Microbiology, 142 ( Pt 2), 217-30 (1996)
- [38] M. H. Saier, Jr. and C. E. Ballou: The 6-O-methylglucose-containing lipopolysaccharide of Mycobacterium phlei. Identification of D-glyceric acid and 3-O-methyl-D-glucose in the polysaccharide. J Biol Chem, 243(5), 992-1005 (1968)
- [39] X. M. He and H. W. Liu: Formation of unusual sugars: mechanistic studies and biosynthetic applications. Annu Rev Biochem, 71, 701-54 (2002)
- [40] C. Kumar, K. Yadav, G. Archana and G. Naresh Kumar: 2-ketogluconic acid secretion by incorporation of Pseudomonas putida KT 2440 gluconate dehydrogenase (gad) operon in Enterobacter asburiae PSI3 improves mineral phosphate solubilization. Curr Microbiol, 67(3), 388-94 (2013) d
- [41] B. L. Moller: Functional diversifications of cyanogenic glucosides. Curr Opin Plant Biol, 13(3), 338-47 (2010)
- [42] F. M. Xi, C. T. Li, J. L. Mi, Z. J. Wu and W. S. Chen: Three new olean-type triterpenoid saponins from aerial parts of Eclipta prostrata (L.). Nat Prod Res, 28(1), 35-40 (2014)
- [43] Z. Zhang, M. R. Yen and M. H. Saier, Jr.: Precise excision of IS5 from the intergenic region between the fucPIK and the fucAO operons and mutational control of fucPIK operon expression in Escherichia coli. J Bacteriol, 192(7), 2013-9 (2010)
- [44] C. K. Holtman, A. C. Pawlyk, N. Meadow, S. Roseman and D. W. Pettigrew: IIA(Glc) allosteric control of Escherichia coli glycerol kinase: binding site cooperative transitions and cation-promoted association by Zinc(II). Biochemistry, 40(47), 14302-8 (2001)
- [45] B. U. Feucht and M. H. Saier, Jr.: Fine control of adenylate cyclase by the phosphoenolpyruvate:sugar phosphotransferase systems in Escherichia coli and Salmonella typhimurium. J Bacteriol, 141(2), 603-10 (1980)
- [46] M. H. Saier, Jr.: The bacterial chromosome. Crit Rev Biochem Mol Biol, 43(2), 89-134 (2008)
- [47] M. S. Wright, A. Iovleva, M. R. Jacobs, R. A. Bonomo and M. D. Adams: Genome dynamics of multidrug-resistant Acinetobacter baumannii during infection and treatment. Genome Med, 8(1), 26 (2016)
- [48] X. Wang and T. K. Wood: IS5 inserts upstream of the master motility operon flhDC in a quasi-Lamarckian way. ISME J, 5(9), 1517-25 (2011)
- [49] M. Kricker and B. G. Hall: Directed evolution of cellobiose utilization in Escherichia coli K12. Mol Biol Evol, 1(2), 171-82 (1984)
- [50] B. G. Hall: On alternatives to selection-induced mutation in the Bgl operon of Escherichia coli. Mol Biol Evol, 11(2), 159-68 (1994)
- [51] B. G. Hall: On the specificity of adaptive mutations. Genetics, 145(1), 39-44 (1997)
- [52] B. G. Hall: Transposable elements as activators of cryptic genes in E. coli. Genetica, 107(1-3), 181-7 (1999)
- [53] J. Vandecraen, P. Monsieurs, M. Mergeay, N. Leys, A. Aertsen and R. Van Houdt: Zinc-Induced Transposition of Insertion Sequence Elements Contributes to Increased Adaptability of Cupriavidus metallidurans. Front Microbiol, 7, 359 (2016)
- [54] T. T. Tseng, K. S. Gratwick, J. Kollman, D. Park, D. H. Nies, A. Goffeau and M. H. Saier, Jr.: The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J Mol Microbiol Biotechnol, 1(1), 107-25 (1999)
- [55] R. A. Elbarbary, B. A. Lucas and L. E. Maquat: Retrotransposons as regulators of gene expression. Science, 351(6274), aac7247 (2016)
- [56] R. A. Watson and E. Szathmary: How Can Evolution Learn? Trends Ecol Evol, 31(2), 147-57 (2016)
