DNA is a fundamentally important molecule for all cellular organisms due to its biological role as the store of hereditary, genetic information. On the one hand, genomic DNA is very stable, both in chemical and biological contexts, and this assists its genetic functions. On the other hand, it is also a dynamic molecule, and constant changes in its structure and sequence drive many biological processes, including adaptation and evolution of organisms. DNA genomes contain significant amounts of repetitive sequences, which have divergent functions in the complex processes that involve DNA, including replication, recombination, repair, and transcription. Through their involvement in these processes, repetitive DNA sequences influence the genetic instability and evolution of DNA molecules and they are located non-randomly in all genomes. Mechanisms that influence such genetic instability have been studied in many organisms, including within human genomes where they are linked to various human diseases. Here, we review our understanding of short, simple DNA repeats across a diverse range of bacteria, comparing the prevalence of repetitive DNA sequences in different genomes. We describe the range of DNA structures that have been observed in such repeats, focusing on their propensity to form local, non-B-DNA structures. Finally, we discuss the biological significance of such unusual DNA structures and relate this to studies where the impacts of DNA metabolism on genetic stability are linked to human diseases. Overall, we show that simple DNA repeats in bacteria serve as excellent and tractable experimental models for biochemical studies of their cellular functions and influences.

Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 612 65 Brno Czech Republic

School of Biological Sciences University of East Anglia Norwich Research Park Norwich NR4 7TJ U K

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Castelle C.J. and Banfield J.F. (2018) Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell 172, 1181–1197 10.1016/j.cell.2018.02.016 PubMed DOI

Kashi Y. and King D.G. (2006) Simple sequence repeats as advantageous mutators in evolution. Trends Genet. 22, 253–259 10.1016/j.tig.2006.03.005 PubMed DOI

Treangen T.J. and Salzberg S.L. (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat. Rev. Genet. 13, 36–46 10.1038/nrg3117 PubMed DOI PMC

Schlötterer C. (2016) Simple repeats. In eLS, John Wiley & Sons, Ltd; (Ed.) 10.1002/9780470015902.a0005066.pub2 DOI

Mrazek J., Guo X. and Shah A. (2007) Simple sequence repeats in prokaryotic genomes. Proc. Natl Acad. Sci. U.S.A. 104, 8472–8477 10.1073/pnas.0702412104 PubMed DOI PMC

van Belkum A., Scherer S., van Alphen L. and Verbrugh H. (1998) Short-sequence DNA repeats in prokaryotic genomes. Microbiol. Mol. Biol. Rev. 62, 275–293 10.1128/MMBR.62.2.275-293.1998 PubMed DOI PMC

Neil A.J., Kim J.C. and Mirkin S.M. (2017) Precarious maintenance of simple DNA repeats in eukaryotes. Bioessays 39, 1700077 10.1002/bies.201700077 PubMed DOI PMC

Bowater R.P. and Waller Z.A. (2014) DNA structure. In eLS, John Wiley & Sons, Ltd; (Ed.) 10.1002/9780470015902.a0006002.pub2 DOI

Ohshima K., Kang S., Larson J.E. and Wells R.D. (1996) Cloning, characterisation, and properties of seven triplet repeat DNA sequences. J. Biol. Chem. 271, 16773–16783 10.1074/jbc.271.28.16773 PubMed DOI

Brazda V., Laister R.C., Jagelska E.B. and Arrowsmith C. (2011) Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol. Biol. 12, 33 10.1186/1471-2199-12-33 PubMed DOI PMC

Blattner F.R., Plunkett I., Bloch G., Perna C.A., Burland N.T., Riley V., (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1462 10.1126/science.277.5331.1453 PubMed DOI

Chen C.W., Huang C.H., Lee H.H., Tsai H.H. and Kirby R. (2002) Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet. 18, 522–529 10.1016/S0168-9525(02)02752-X PubMed DOI

Hopwood D.A. (2006) Soil to genomics: the streptomyces chromosome. Ann. Rev. Genet. 40, 1–23 10.1146/annurev.genet.40.110405.090639 PubMed DOI

Toth G., Gaspari Z. and Jurka J. (2000) Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res. 10, 967–981 10.1101/gr.10.7.967 PubMed DOI PMC

Field D. and Wills C. (1998) Abundant microsatellite polymorphism in Saccharomyces cerevisiae, and the different distributions of microsatellites in eight prokaryotes and S. cerevisiae, result from strong mutation pressures and a variety of selective forces. Proc. Natl Acad. Sci. U.S.A. 95, 1647–1652 10.1073/pnas.95.4.1647 PubMed DOI PMC

Mrazek J. (2006) Analysis of distribution indicates diverse functions of simple sequence repeats in Mycoplasma genomes. Mol. Biol. Evol. 23, 1370–1385 10.1093/molbev/msk023 PubMed DOI

Benson G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573–580 10.1093/nar/27.2.573 PubMed DOI PMC

Gur-Arie R., Cohen C.J., Eitan Y., Shelef L., Hallerman E.M. and Kashi Y. (2000) Simple sequence repeats in Escherichia coli: abundance, distribution, composition, and polymorphism. Genome Res. 10, 62–71 PMID: PubMed PMC

Kryukov K., Sumiyama K., Ikeo K., Gojobori T. and Saitou N. (2012) A new database (GCD) on genome composition for eukaryote and prokaryote genome sequences and their initial analyses. Genome Biol. Evol. 4, 501–512 10.1093/gbe/evs026 PubMed DOI PMC

Wu H., Zhang Z., Hu S. and Yu J. (2012) On the molecular mechanism of GC content variation among eubacterial genomes. Biol. Direct 7, 2 10.1186/1745-6150-7-2 PubMed DOI PMC

Bhagwat A.S. and Lieb M. (2002) Cooperation and competition in mismatch repair: very short-patch repair and methyl-directed mismatch repair in Escherichia coli. Mol. Microbiol. 44, 1421–1428 10.1046/j.1365-2958.2002.02989.x PubMed DOI

Aksenova A.Y. and Mirkin S.M. (2019) At the beginning of the end and in the middle of the beginning: structure and maintenance of telomeric DNA repeats and interstitial telomeric sequences. Genes 10, E118 10.3390/genes10020118 PubMed DOI PMC

Metzgar D., Thomas E., Davis C., Field D. and Wills C. (2001) The microsatellites of Escherichia coli: rapidly evolving repetitive DNAs in a non-pathogenic prokaryote. Mol. Microbiol. 39, 183–190 10.1046/j.1365-2958.2001.02245.x PubMed DOI

van Belkum A. (2007) Tracing isolates of bacterial species by multilocus variable number of tandem repeat analysis (MLVA). FEMS Immunol. Med. Microbiol. 49, 22–27 10.1111/j.1574-695X.2006.00173.x PubMed DOI

Dyet K.H., Robertson I., Turbitt E. and Carter P.E. (2011) Characterization of Escherichia coli O157:H7 in New Zealand using multiple-locus variable-number tandem-repeat analysis. Epidemiol. Infect 139, 464–471 10.1017/S0950268810001068 PubMed DOI

Byrne L., Elson R., Dallman T.J., Perry N., Ashton P., Wain J. et al. (2014) Evaluating the use of multilocus variable number tandem repeat analysis of Shiga toxin-producing Escherichia coli O157 as a routine public health tool in England. PLoS One 9, e85901 10.1371/journal.pone.0085901 PubMed DOI PMC

Melles D.C., Schouls L., Francois P., Herzig S., Verbrugh H.A., van Belkum A. et al. (2009) High-throughput typing of Staphylococcus aureus by amplified fragment length polymorphism (AFLP) or multi-locus variable number of tandem repeat analysis (MLVA) reveals consistent strain relatedness. Eur. J. Clin. Microbiol. Infect. Dis. 28, 39–45 10.1007/s10096-008-0585-4 PubMed DOI

Mohanty P.S., Bansal A.K., Naaz F., Arora M., Gupta U.D., Gupta P. et al. (2019) Multiple strain infection of Mycobacterium leprae in a family having 4 patients: a study employing short tandem repeats. PLoS One 14, e0214051 10.1371/journal.pone.0214051 PubMed DOI PMC

Bowater R.P., Chen D. and Lilley D.M.J. (1994) Elevated unconstrained supercoiling of plasmid DNA generated by transcription and translation of the tetracycline resistance gene in eubacteria. Biochemistry 33, 9266–9275 10.1021/bi00197a030 PubMed DOI

Hatfield G.W. and Benham C.J. (2002) DNA topology-mediated control of global gene expression in Escherichia coli. Annu. Rev. Genet. 36, 175–203 10.1146/annurev.genet.36.032902.111815 PubMed DOI

Pearson C.E., Edamura K.N. and Cleary J.D. (2005) Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet. 6, 729–742 10.1038/nrg1689 PubMed DOI

Mirkin S.M. (2006) DNA structures, repeat expansions and human hereditary disorders. Curr. Opin. Struct. Biol. 16, 351–358 10.1016/j.sbi.2006.05.004 PubMed DOI

Wells R.D. (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci. 32, 271–278 10.1016/j.tibs.2007.04.003 PubMed DOI

Sjakste T., Paramonova N. and Sjakste N. (2016) Structural and functional significance of microsatellites. Biopolym. Cell 32, 334–346 10.7124/bc.000930 DOI

McClellan J.A., Boublikova P., Palecek E. and Lilley D.M.J. (1990) Superhelical torsion in cellular DNA responds directly to environmental and genetic factors. Proc. Natl Acad. Sci. U.S.A. 87, 8373–8377 10.1073/pnas.87.21.8373 PubMed DOI PMC

Gimenes F., Takeda K.I., Fiorini A., Gouveia F.S. and Fernandez M.A. (2008) Intrinsically bent DNA in replication origins and gene promoters. Genet. Mol. Res 7, 549–558 10.4238/vol7-2gmr461 PubMed DOI

Murat P. and Balasubramanian S. (2014) Existence and consequences of G-quadruplex structures in DNA. Curr. Opin. Genet. Dev. 25, 22–29 10.1016/j.gde.2013.10.012 PubMed DOI

Mitas M. (1997) Trinucleotide repeats associated with human disease. Nucleic Acids Res. 25, 2245–2254 10.1093/nar/25.12.2245 PubMed DOI PMC

Kiliszek A. and Rypniewski W. (2014) Structural studies of CNG repeats. Nucleic Acids Res. 42, 8189–8199 10.1093/nar/gku536 PubMed DOI PMC

Wang G. and Vasquez K.M. (2007) Z-DNA, an active element in the genome. Front Biosci. 12, 4424–4438 10.2741/2399 PubMed DOI

Bochman M.L., Paeschke K. and Zakian V.A. (2012) DNA secondary structures: stability and function of G-quadruplex structures. Nat. Rev. Genet. 13, 770–780 10.1038/nrg3296 PubMed DOI PMC

Malgowska M., Gudanis D., Kierzek R., Wyszko E., Gabelica V. and Gdaniec Z. (2014) Distinctive structural motifs of RNA G-quadruplexes composed of AGG, CGG and UGG trinucleotide repeats. Nucleic Acids Res. 42, 10196–101207 10.1093/nar/gku710 PubMed DOI PMC

Zamiri B., Mirceta M., Bomsztyk K., Macgregor R.B. Jr. and Pearson C.E. (2015) Quadruplex formation by both G-rich and C-rich DNA strands of the C9orf72 (GGGGCC)8*(GGCCCC)8 repeat: effect of CpG methylation. Nucleic Acids Res. 43, 10055–10064 10.1093/nar/gkv1008 PubMed DOI PMC

Cheng M., Cheng Y., Hao J., Jia G., Zhou J., Mergny J.L. et al. (2018) Loop permutation affects the topology and stability of G-quadruplexes. Nucleic Acids Res. 46, 9264–9275 10.1093/nar/gky757 PubMed DOI PMC

Bartas M., Cutova M., Brazda V., Kaura P., Stastny J., Kolomaznik J., et al. (2019) The presence and localization of G-quadruplex forming sequences in the domain of bacteria. Molecules 24, 1711 10.3390/molecules24091711 PubMed DOI PMC

McRae E.K.S., Booy E.P., Padilla-Meier G.P. and McKenna S.A. (2017) On characterizing the interactions between proteins and guanine quadruplex structures of nucleic acids. J. Nucleic Acids 2017, 9675348 10.1155/2017/9675348 PubMed DOI PMC

Qiu J., Liu J., Chen S., Ou T.M., Tan J.H., Gu L.Q. et al. (2015) Role of Hairpin-Quadruplex DNA secondary structural conversion in the promoter of hnRNP K in gene transcriptional regulation. Org. Lett. 17, 4584–4587 10.1021/acs.orglett.5b02310 PubMed DOI

Abdelhamid M.A., Fabian L., MacDonald C.J., Cheesman M.R., Gates A.J. and Waller Z.A. (2018) Redox-dependent control of i-Motif DNA structure using copper cations. Nucleic Acids Res. 46, 5886–5893 10.1093/nar/gky390 PubMed DOI PMC

Dembska A., Bielecka P. and Juskowiak B. (2017) pH-Sensing fluorescence oligonucleotide probes based on an i-motif scaffold: a review. Anal. Methods 9, 6092–6106 10.1039/C7AY01942D DOI

Abou Assi H., Garavis M., Gonzalez C. and Damha M.J. (2018) i-Motif DNA: structural features and significance to cell biology. Nucleic Acids Res. 46, 8038–8056 10.1093/nar/gky735 PubMed DOI PMC

Wright E.P., Huppert J.L. and Waller Z.A.E. (2017) Identification of multiple genomic DNA sequences which form i-motif structures at neutral pH. Nucleic Acids Res. 45, 2951–2959 10.1093/nar/gkx090 PubMed DOI PMC

Fojtik P., Kejnovska I. and Vorlickova M. (2004) The guanine-rich fragile X chromosome repeats are reluctant to form tetraplexes. Nucleic Acids Res. 32, 298–306 10.1093/nar/gkh179 PubMed DOI PMC

Renciuk D., Zemanek M., Kejnovska I. and Vorlickova M. (2009) Quadruplex-forming properties of FRAXA (CGG) repeats interrupted by (AGG) triplets. Biochimie 91, 416–422 10.1016/j.biochi.2008.10.012 PubMed DOI

Schmidt M.H. and Pearson C.E. (2016) Disease-associated repeat instability and mismatch repair. DNA Repair (Amst.) 38, 117–126 10.1016/j.dnarep.2015.11.008 PubMed DOI

Freudenreich C.H. (2018) R-loops: targets for nuclease cleavage and repeat instability. Curr. Genet. 64, 789–794 10.1007/s00294-018-0806-z PubMed DOI PMC

Kumari D., Lokanga R., Yudkin D., Zhao X.N. and Usdin K. (2012) Chromatin changes in the development and pathology of the Fragile X-associated disorders and Friedreich ataxia. Biochim. Biophys. Acta 1819, 802–810 10.1016/j.bbagrm.2011.12.009 PubMed DOI PMC

Wang G. and Vasquez K.M. (2014) Impact of alternative DNA structures on DNA damage, DNA repair, and genetic instability. DNA Repair (Amst.) 19, 143–151 10.1016/j.dnarep.2014.03.017 PubMed DOI PMC

Bacolla A. and Wells R.D. (2009) Non-B DNA conformations as determinants of mutagenesis and human disease. Molecular Carcinog. 48, 273–285 10.1002/mc.20507 PubMed DOI

Rocha E.P. (2008) The organization of the bacterial genome. Annu. Rev. Genet. 42, 211–233 10.1146/annurev.genet.42.110807.091653 PubMed DOI

West B.J., Allegrini P., Buiatti M. and Grigolini P. (2000) Non-normal statistics of DNA sequences of prokaryotes. J. Biol. Phys. 26, 17–25 10.1023/A:1005284418550 PubMed DOI PMC

Jansen R., Embden J.D., Gaastra W. and Schouls L.M. (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43, 1565–1575 10.1046/j.1365-2958.2002.02839.x PubMed DOI

Kolsto A.B. (1997) Dynamic bacterial genome organization. Mol. Microbiol. 24, 241–248 10.1046/j.1365-2958.1997.3501715.x PubMed DOI

Cechova J., Lysek J., Bartas M. and Brazda V. (2017) Complex analyses of inverted repeats in mitochondrial genomes revealed their importance and variability. Bioinformatics 34, 1081–1085 10.1093/bioinformatics/btx729 PubMed DOI PMC

Brazda V., Lysek J., Bartas M. and Fojta M. (2018) Complex analyses of short inverted repeats in all sequenced chloroplast DNAs. Biomed. Res. Int. 2018, 1097018 10.1155/2018/1097018 PubMed DOI PMC

Horwitz M.S. and Loeb L.A. (1988) An E. coli promoter that regulates transcription by DNA superhelix-induced cruciform extrusion. Science 241, 703–705 10.1126/science.2456617 PubMed DOI

Holder I.T., Wagner S., Xiong P., Sinn M., Frickey T., Meyer A. et al. (2015) Intrastrand triplex DNA repeats in bacteria: a source of genomic instability. Nucleic Acids Res. 43, 10126–10142 10.1093/nar/gkv1017 PubMed DOI PMC

Bacolla A., Wang G. and Vasquez K.M. (2015) New perspectives on DNA and RNA triplexes as effectors of biological activity. PLoS Genet. 11, e1005696 10.1371/journal.pgen.1005696 PubMed DOI PMC

Kikin O., D'Antonio L. and Bagga P.S. (2006) QGRS mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res. 34, W676–W682 10.1093/nar/gkl253 PubMed DOI PMC

Brazda V., Kolomaznik J., Lysek J., Bartas M., Fojta M., Stastny J. et al. (2019) G4hunter web application: a web server for G-quadruplex prediction. Bioinformatics 35, 3493–3495 10.1093/bioinformatics/btz087 PubMed DOI PMC

Yadav V.K., Abraham J.K., Mani P., Kulshrestha R. and Chowdhury S. (2008) Quadbase: genome-wide database of G4 DNA-occurrence and conservation in human, chimpanzee, mouse and rat promoters and 146 microbes. Nucleic Acids Res. 36, D381–D385 10.1093/nar/gkm781 PubMed DOI PMC

Dhapola P. and Chowdhury S. (2016) Quadbase2: web server for multiplexed guanine quadruplex mining and visualization. Nucleic Acids Res. 44, W277–W283 10.1093/nar/gkw425 PubMed DOI PMC

Rawal P., Kummarasetti V.B., Ravindran J., Kumar N., Halder K., Sharma R. et al. (2006) Genome-wide prediction of G4 DNA as regulatory motifs: role in Escherichia coli global regulation. Genome Res. 16, 644–655 10.1101/gr.4508806 PubMed DOI PMC

Brazda V., Haronikova L., Liao J.C. and Fojta M. (2014) DNA and RNA quadruplex-binding proteins. Int. J. Mol. Sci. 15, 17493–17517 10.3390/ijms151017493 PubMed DOI PMC

Day H.A., Pavlou P. and Waller Z.A. (2014) i-Motif DNA: structure, stability and targeting with ligands. Bioorg. Med. Chem. 22, 4407–4418 10.1016/j.bmc.2014.05.047 PubMed DOI

Harris L.M. and Merrick C.J. (2015) G-quadruplexes in pathogens: a common route to virulence control? PLoS Pathog. 11, e1004562 10.1371/journal.ppat.1004562 PubMed DOI PMC

Rhodes D. and Lipps H.J. (2015) G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 43, 8627–8637 10.1093/nar/gkv862 PubMed DOI PMC

Saranathan N. and Vivekanandan P. (2019) G-quadruplexes: more than just a kink in microbial genomes. Trends Microbiol. 27, 148–163 10.1016/j.tim.2018.08.011 PubMed DOI PMC

Day H.A., Wright E.P., MacDonald C.J., Gates A.J. and Waller Z.A. (2015) Reversible DNA i-motif to hairpin switching induced by copper(II) cations. Chem. Commun. (Camb.) 51, 14099–14102 10.1039/C5CC05111H PubMed DOI PMC

Waller Z.A., Pinchbeck B.J., Buguth B.S., Meadows T.G., Richardson D.J. and Gates A.J. (2016) Control of bacterial nitrate assimilation by stabilization of G-quadruplex DNA. Chem. Commun. (Camb.) 52, 13511–4 10.1039/C6CC06057A PubMed DOI PMC

Abdelhamid M.A.S., Gates A.J. and Waller Z.A.E. (2019) Destabilization of i-Motif DNA at neutral pH by G-quadruplex ligands. Biochemistry 58, 245–249 10.1021/acs.biochem.8b00968 PubMed DOI

Pinchbeck B.J., Soriano-Laguna M.J., Sullivan M.J., Luque-Almagro V.M., Rowley G., Ferguson S.J. et al. (2019) A dual functional redox enzyme maturation protein for respiratory and assimilatory nitrate reductases in bacteria. Mol. Microbiol. 111, 1592–1603 10.1111/mmi.14239 PubMed DOI PMC

Iyer R.R., Pluciennik A., Napierala M. and Wells R.D. (2015) DNA triplet repeat expansion and mismatch repair. Annu. Rev. Biochem. 84, 199–226 10.1146/annurev-biochem-060614-034010 PubMed DOI PMC

Chatterjee N. and Walker G.C. (2017) Mechanisms of DNA damage, repair, and mutagenesis. Environ. Mol. Mutagen. 58, 235–263 10.1002/em.22087 PubMed DOI PMC

Shah K.A. and Mirkin S.M. (2015) The hidden side of unstable DNA repeats: mutagenesis at a distance. DNA Repair (Amst.) 32, 106–112 10.1016/j.dnarep.2015.04.020 PubMed DOI PMC

Lahue R.S. and Slater D.L. (2003) DNA repair and trinucleotide repeat instability. Front. Biosci. 8, s653–s665 10.2741/1107 PubMed DOI

Zhao X.N. and Usdin K. (2015) The repeat expansion diseases: the dark side of DNA repair. DNA Repair (Amst.) 32, 96–105 10.1016/j.dnarep.2015.04.019 PubMed DOI PMC

Bowater R.P. and Wells R.D. (2001) The intrinsically unstable life of DNA triplet repeats associated with human hereditary disorders. Prog. Nucleic Acids Res. Mol. Biol. 66, 159–202 10.1016/S0079-6603(00)66029-4 PubMed DOI

Krasilnikova M., Samadashwily G.M., Krasilnikov A.S. and Mirkin S.M. (1998) Transcription through a simple DNA repeat blocks replication elongation. EMBO J. 17, 5095–5102 10.1093/emboj/17.17.5095 PubMed DOI PMC

Bowater R.P., Jaworski A., Larson J.E., Parniewski P. and Wells R.D. (1997) Transcription increases the deletion frequency of long CTG•CAG triplet repeats from plasmids in Escherichia coli. Nucleic Acids Res. 25, 2861–2868 10.1093/nar/25.14.2861 PubMed DOI PMC

Lin Y., Dent S.Y., Wilson J.H., Wells R.D. and Napierala M. (2010) R loops stimulate genetic instability of CTG.CAG repeats. Proc. Natl Acad. Sci. U.S.A. 107, 692–697 10.1073/pnas.0909740107 PubMed DOI PMC

Reddy K., Tam M., Bowater R.P., Barber M., Tomlinson M., Nichol Edamura K. et al. (2011) Determinants of R-loop formation at convergent bidirectionally transcribed trinucleotide repeats. Nucleic Acids Res. 39, 1749–1762 10.1093/nar/gkq935 PubMed DOI PMC

Zhao J., Bacolla A., Wang G. and Vasquez K.M. (2010) Non-B DNA structure-induced genetic instability and evolution. Cell. Mol. Life Sci. 67, 43–62 10.1007/s00018-009-0131-2 PubMed DOI PMC

Hoeijmakers J.H. (2001) Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374 10.1038/35077232 PubMed DOI

Friedberg E.C. (2003) DNA damage and repair. Nature 421, 436–440 10.1038/nature01408 PubMed DOI

Gorna A.E., Bowater R.P. and Dziadek J. (2010) DNA repair systems and the pathogenesis of Mycobacterium tuberculosis: varying activities at different stages of infection. Clin Sci (Lond) 119, 187–202 10.1042/CS20100041 PubMed DOI

van der Veen S. and Tang C.M. (2015) The BER necessities: the repair of DNA damage in human-adapted bacterial pathogens. Nat. Rev. Microbiol. 13, 83–94 10.1038/nrmicro3391 PubMed DOI

Uphoff S. and Sherratt D.J. (2017) Single-molecule analysis of bacterial DNA repair and mutagenesis. Annu. Rev. Biophys. 46, 411–432 10.1146/annurev-biophys-070816-034106 PubMed DOI

Loeb K.R. and Loeb L.A. (1999) Genetic instability and the mutator phenotype. Am. J. Pathol. 154, 1621–1626 10.1016/S0002-9440(10)65415-6 PubMed DOI PMC

Bacolla A., Wojciechowska M., Kosmider B., Larson J.E. and Wells R.D. (2006) The involvement of non-B DNA structures in gross chromosomal rearrangements. DNA Repair (Amst.) 5, 1161–1170 10.1016/j.dnarep.2006.05.032 PubMed DOI

Wojcik E.A., Brzostek A., Bacolla A., Mackiewicz P., Vasquez K.M., Korycka-Machala M. et al. (2012) Direct and inverted repeats elicit genetic instability by both exploiting and eluding DNA double-strand break repair systems in mycobacteria. PLoS One 7, e51064 10.1371/journal.pone.0051064 PubMed DOI PMC

Mendoza O., Bourdoncle A., Boule J.B., Brosh R.M. Jr. and Mergny J.L. (2016) G-quadruplexes and helicases. Nucleic Acids Res. 44, 1989–2006 10.1093/nar/gkw079 PubMed DOI PMC

Shen J.C. and Loeb L.A. (2000) The Werner syndrome gene: the molecular basis of RecQ helicase-deficiency diseases. Trends Genet. 16, 213–220 10.1016/S0168-9525(99)01970-8 PubMed DOI

Wu X. and Maizels N. (2001) Substrate-specific inhibition of RecQ helicase. Nucleic Acids Res. 29, 1765–1771 10.1093/nar/29.8.1765 PubMed DOI PMC

Moxon R., Bayliss C. and Hood D. (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu. Rev. Genet. 40, 307–333 10.1146/annurev.genet.40.110405.090442 PubMed DOI

Kashi Y., King D. and Soller M. (1997) Simple sequence repeats as a source of quantitative genetic variation. Trends Genet. 13, 74–78 10.1016/S0168-9525(97)01008-1 PubMed DOI

Karlin S., Campbell A.M. and Mrazek J. (1998) Comparative DNA analysis across diverse genomes. Annu. Rev. Genet. 32, 185–225 10.1146/annurev.genet.32.1.185 PubMed DOI

Groisman E.A. and Casadesus J. (2005) The origin and evolution of human pathogens. Mol. Microbiol. 56, 1–7 10.1111/j.1365-2958.2005.04564.x PubMed DOI

Power P.M., Sweetman W.A., Gallacher N.J., Woodhall M.R., Kumar G.A., Moxon E.R. et al. (2009) Simple sequence repeats in Haemophilus influenzae. Infect. Genet. Evol. 9, 216–228 10.1016/j.meegid.2008.11.006 PubMed DOI PMC

Zhou K., Aertsen A. and Michiels C.W. (2014) The role of variable DNA tandem repeats in bacterial adaptation. FEMS Microbiol. Rev. 38, 119–141 10.1111/1574-6976.12036 PubMed DOI

Peak I.R., Jennings M.P., Hood D.W. and Moxon E.R. (1999) Tetranucleotide repeats identify novel virulence determinant homologues in Neisseria meningitidis. Microb. Pathog. 26, 13–23 10.1006/mpat.1998.0243 PubMed DOI

Hood D.W., Deadman M.E., Jennings M.P., Bisercic M., Fleischmann R.D., Venter J.C. et al. (1996) DNA repeats identify novel virulence genes in Haemophilus influenzae. Proc. Natl Acad. Sci. U.S.A. 93, 11121–11215 10.1073/pnas.93.20.11121 PubMed DOI PMC

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