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Toxin-Antitoxin Loci in Streptococcus pneumoniae

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Prokaryotic Toxin-Antitoxins

Abstract

The Gram-positive human pathogen Streptococcus pneumoniae harbours a number of type II toxin–antitoxin loci, three of which have been functionally characterised. The pneumococcal relBE2 and yefM-yoeB TA systems are described here in detail in terms of their genetic organisation, gene regulation and protein structure. A number of putative TA loci with unusual genetic organisations are also presented. The possible roles of the pneumococcal TA loci in persistence and the phenomenon of bistability are discussed.

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Abbreviations

(TAS):

Toxin–antitoxin system(s)

(nt):

Nucleotides

(IR-1 and IR-2):

Inverted repeats

(ORF):

Open reading frame

References

  • Alonso, J. C., Balsa, D., Cherny, I., Christensen, S. K., Espinosa, M., Francuski, D., et al. (2007). Bacterial toxin-antitoxin systems as targets for the development of novel antibiotics. In R. A. Bonomo & M. E. Tolmasky (Eds.), Enzyme-mediated resistance to antibiotics: Mechanisms, dissemination, and prospects for inhibition (pp. 313–329). Washington: ASM Press.

    Google Scholar 

  • Baquero, F. (2004). From pieces to patterns: Evolutionary engineering in bacterial pathogens. Nature Reviews Microbiology, 2, 510–518.

    Article  PubMed  CAS  Google Scholar 

  • Baquero, F. (2009). Environmental stress and evolvability in microbial systems. Clinical Microbiology and Infection, 15, 5–10.

    Article  PubMed  Google Scholar 

  • Basset, A., Turner, K. H., Boush, E., Sayeed, S., Dove, S. L., & Malley, R. (2012). An epigenetic switch mediates bistable expression of the type 1 pilus genes in Streptococcus pneumoniae. Journal of Bacteriology, 194, 1088–1091.

    Article  PubMed  CAS  Google Scholar 

  • Bogaert, D., van Belkum, A., Sluijter, M., Luijendijk, A., de Groot, R., Rümke, H. C., et al. (2004). Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet, 363, 1871–1872.

    Article  PubMed  CAS  Google Scholar 

  • Camara, M., Mitchell, T. J., Andrew, P. W., & Boulnois, G. J. (1991). Streptococcus pneumoniae produces at least two distinct enzymes with neuraminidase activity: Cloning and expression of a second neuraminidase gene in Escherichia coli. Infection and Immunity, 59, 2856–2858.

    PubMed  CAS  Google Scholar 

  • Claverys, J. P., & Havarstein, L. S. (2007). Cannibalism and fratricide: Mechanisms and raisons d’être. Nature Reviews Microbiology, 5, 219–229.

    Article  PubMed  CAS  Google Scholar 

  • Claverys, J. P., Prudhomme, M., & Martin, B. (2006). Induction of competence regulons as general stress responses in Gram-positive bacteria. Annual Review of Microbiology, 60, 451–475.

    Article  PubMed  CAS  Google Scholar 

  • Cooper, W. S., & Kaplan, R. H. (1982). Adaptive ‘coin-flipping’: A decision-theoretical examination of natural selection for a random individual variation. Journal of Theoretical Biology, 94, 135–151.

    Article  PubMed  CAS  Google Scholar 

  • Croucher, N. J., Vernikos, G. S., Parkhill, J., & Bentley, S. D. (2011). Identification, variation and transcription of pneumococcal repeat sequences. BMC Genomics, 12, 120.

    Article  PubMed  CAS  Google Scholar 

  • Croucher, N. J., Walker, D. R., Romero, P., Lennard, N., Paterson, G. K., Bason, N. C., et al. (2009). Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniae Spain23F ST81. Journal of Bacteriology, 191, 1480–1489.

    Article  PubMed  CAS  Google Scholar 

  • Chan, W. T., Nieto, C., Harikrishna, J. A., Khoo, S. K., Yasmin Othman, R., Espinosa, M., et al. (2011). Genetic regulation of the yefM-yoeB Spn toxin-antitoxin locus of Streptococcus pneumoniae. Journal of Bacteriology, 193, 4612–4625.

    Article  PubMed  CAS  Google Scholar 

  • Chan, W. T., Moreno-Córdoba, I., Yeo, C. C., & Espinosa, M. (2013). Manuscript in preparation.

    Google Scholar 

  • Chandler, M. S., & Morrison, D. A. (1988). Identification of two proteins encoded by com, a competence control locus of Streptococcus pneumoniae. Journal of Bacteriology, 170, 3136–3141.

    PubMed  CAS  Google Scholar 

  • Cherny, I., Overgaard, M., Borch, J., Bram, Y., Gerdes, K., & Gazit, E. (2007). Structural and thermodynamic characterization of the Escherichia coli RelBE toxin-antitoxin system: Indication for a functional role of differential stability. Biochemistry, 46, 12152–12163.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, K. S., Maenhauf-Michel, G., Mine, N., Gothesman, S., Gerdes, K., & Van Melderen, L. (2004). Overproduction of the Lon protease triggers inhibition of translation in Escherichia coli: Involvement of the yefM-yoeB toxin-antitoxin system. Molecular Microbiology, 51, 1705–1717.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, S. K., & Gerdes, K. (2003). RelE toxins from bacteria and archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Molecular Microbiology, 48, 1389–1400.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, S. K., & Gerdes, K. (2004). Delayed-relaxed response explained by hyperactivation of RelE. Molecular Microbiology, 53, 587–597.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, S. K., Mikkelsen, M., Pedersen, K., & Gerdes, K. (2001). RelE, a global inhibitor of translation, is activated during nutritional stress. Proceedings of the National academy of Sciences of the United States of America, 98, 14328–14333.

    Article  PubMed  CAS  Google Scholar 

  • del Solar, G., Hernández-Arriaga, A. M., Gomis-Rüth, F. X., Coll, M., & Espinosa, M. (2002). A genetically economical family of plasmid-encoded transcriptional repressors in control of plasmid copy number. Journal of Bacteriology, 184, 4943–4951.

    Article  PubMed  Google Scholar 

  • Dubnau, D., & Losick, R. (2006). Bistability in bacteria. Molecular Microbiology, 61, 564–572.

    Article  PubMed  CAS  Google Scholar 

  • Elowitz, M. B., Levine, A. J., Siggia, E. D., & Swain, P. S. (2002). Stochastic gene expression in a single cell. Science, 297, 1183–1186.

    Article  PubMed  CAS  Google Scholar 

  • Engelberg-Kulka, H., & Glaser, G. (1999). Addiction modules and programmed cell death and antideath in bacterial cultures. Annual Review of Microbiology, 53, 43–70.

    Article  PubMed  CAS  Google Scholar 

  • Epstein, S. S. (2009). Microbial awakenings. Nature, 457, 1083.

    Article  PubMed  CAS  Google Scholar 

  • Evdokimov, A., Voznesensky, I., Fennell, K., Anderson, M., Smith, J. F., & Fisher, D. A. (2009). New kinase regulation mechanism found in HipBA: A bacterial persistence switch. Acta Crystallographica. Section D, Biological Crystallography, 65, 875–879.

    Article  PubMed  Google Scholar 

  • Francuski, D., & Saenger, W. (2009). Crystal structure of the antitoxin-toxin protein complex RelB-RelE from Methanococcus jannaschii. Journal of Molecular Biology, 393, 898–908.

    Article  PubMed  CAS  Google Scholar 

  • Gaál, B., Pitchford, J. W., & Wood, A. J. (2010). Exact results for the evolution of stochastic switching in variable asymmetric environments. Genetics, 184, 1113–1119.

    Article  PubMed  Google Scholar 

  • Gamez, G., & Hammerschmidt, S. (2012). Combat pneumococcal infections: Adhesins as candidates for protein-based vaccine development. Current Drug Targets, 13, 323–337.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Pino, A., Christensen-Dalsgaard, M., Wyns, L., Yarmolinsky, M. B., Magnuson, R. D., Gerdes, K., et al. (2008). Doc of prophage P1 is inhibited by its antitoxin partner Phd through fold complementation. Journal of Biological Chemistry, 283, 30821–30827.

    Article  PubMed  CAS  Google Scholar 

  • Gomis-Ruth, F. X., Sola, M., Acebo, P., Parraga, A., Guasch, A., Eritja, R., et al. (1998). The structure of plasmid-encoded transcriptional repressor CopG unliganded and bound to its operator. EMBO Journal, 17, 7404–7415.

    Article  PubMed  CAS  Google Scholar 

  • Gotfredsen, M., & Gerdes, K. (1998). The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Molecular Microbiology, 29, 1065–1076.

    Article  PubMed  CAS  Google Scholar 

  • Gronlund, H., & Gerdes, K. (1999). Toxin-antitoxin systems homologous with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. Journal of Molecular Biology, 285, 1401–1415.

    Article  PubMed  CAS  Google Scholar 

  • Hanage, W. P., Fraser, C., Tang, J., Connor, T. R., & Corander, J. (2009). Hyper-Recombination, diversity, and antibiotic resistance in pneumococcus. Science, 324, 1454–1457.

    Article  PubMed  CAS  Google Scholar 

  • Heinrich, J., Velleman, M., & Schuster, H. (1995). The tripartite immunity system of phages P1 and P7. FEMS Microbiology Reviews, 17, 121–126.

    Article  PubMed  CAS  Google Scholar 

  • Hoskins, J., Alborn, W. E, Jr, Arnold, J., Blaszczak, L. C., Burgett, S., DeHoff, B. S., et al. (2001). Genome of the bacterium Streptococcus pneumoniae strain R6. Journal of Bacteriology, 183, 5709–5717.

    Article  PubMed  CAS  Google Scholar 

  • Hurley, J. M., Cruz, J. W., Ouyang, M., & Woychik, N. A. (2011). Bacterial toxin RelE mediates frequent codon-independent mRNA cleavage from the 5′ end of coding regions in vivo. Journal of Biological Chemistry, 286, 14770–14778.

    Article  PubMed  CAS  Google Scholar 

  • Iyer, L.M., Koonin, E.V., Aravind, L. (2002). Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal APSES transcription factors. Genome Biologyl, 3, RESEARCH0012.

    Google Scholar 

  • Kadioglu, A., Weiser, J. N., Paton, J. C., & Andrew, P. W. (2008). The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nature Reviews Microbiology, 6, 288–301.

    Article  PubMed  CAS  Google Scholar 

  • Kamada, K., & Hanaoka, F. (2005). Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Molecular Cell, 19, 497–509.

    Article  PubMed  CAS  Google Scholar 

  • Keren, I., Shah, D., Spoering, A., Kaldalu, N., & Lewis, K. (2004). Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. Journal of Bacteriology, 186, 8172–8180.

    Article  PubMed  CAS  Google Scholar 

  • Khoo, S. K., Loll, B., Chan, W. T., Shoeman, R. L., Ngoo, L., Yeo, C. C., et al. (2007). Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae. Journal of Biological Chemistry, 282, 19606–19618.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y., Wang, X., Ma, Q., Zhang, X. S., & Wood, T. K. (2009). Toxin-antitoxin systems in Escherichia coli influence biofilm formation through YjgK (TabA) and fimbriae. Journal of Bacteriology, 191, 1258–1267.

    Article  PubMed  CAS  Google Scholar 

  • Knutsen, E., Johnsborg, O., Quentin, Y., Claverys, J. P., & Havarstein, L. S. (2006). BOX elements modulate gene expression in Streptococcus pneumoniae: Impact on the fine-tuning of competence development. Journal of Bacteriology, 188, 8307–8312.

    Article  PubMed  CAS  Google Scholar 

  • Kuchina, A., Espinar, L., Cagatay, T., Balbin, A. O., Zhang, F., Alvarado, A., et al. (2011). Temporal competition between differentiation programs determines cell fate choice. Molecular Systems Biology, 7, 557.

    Article  PubMed  Google Scholar 

  • Kumar, P., Issac, B., Dodson, E. J., Turkenburg, J. P., & Mande, S. C. (2008). Crystal structure of Mycobacterium tuberculosis YefM antitoxin reveals that it is not an intrinsically unstructured protein. Journal of Molecular Biology, 383, 482–493.

    Article  PubMed  CAS  Google Scholar 

  • Kuwahara, H., & Soyer, O. S. (2012). Bistability in feedback circuits as a byproduct of evolution of evolvability. Molecular Systems Biology, 8, 564.

    Article  PubMed  CAS  Google Scholar 

  • Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Drèze, P., & Van Melderen, L. (2011). Diversity of bacterial type II toxin–antitoxin systems: A comprehensive search and functional analysis of novel families. Nucleic Acids Research, 39, 5513–5525.

    Article  PubMed  CAS  Google Scholar 

  • Leung, V., & Lévesque, C. M. (2012). A stress inducible quorum sensing peptide mediates the formation of non-inherited multidrug tolerant persister cells. Journal of Bacteriology, 194, 2265–2274.

    Article  PubMed  CAS  Google Scholar 

  • Li, G.-Y., Zhang, Y., Inouye, M., & Ikura, M. (2008). Structural mechanism of transcriptional autorepression of the Escherichia coli RelB/RelE antitoxin/toxin module. Journal of Molecular Biology, 380, 107–119.

    Article  PubMed  CAS  Google Scholar 

  • Maisonneuve, E., Shakespeare, L. J., Jørgensen, M. G., & Gerdes, K. (2011). Bacterial persistence by RNA endonucleases. Proceedings of the National academy of Sciences of the United States of America, 108, 13206–13211.

    Article  PubMed  CAS  Google Scholar 

  • Makarova, K., Wolf, Y. I., & Koonin, E. V. (2009). Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biology Direct, 4, 19.

    Article  PubMed  Google Scholar 

  • Martin, B., Humbert, O., Camara, M., Guenzi, E., Walker, J. R., Mitchell, T., et al. (1992). A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acid Research, 20, 3479–3483.

    Article  CAS  Google Scholar 

  • Moreno-Córdoba, I., Diago-Navarro, E., Barendregt, A., Heck, A. J. R., Alfonso, C., Díaz-Orejas, R., et al. (2012). The toxin-antitoxin proteins RelBE2Spn of Streptococcus pneumoniae: Characterization and association to their DNA target. Proteins, 80, 1834–1846.

    PubMed  Google Scholar 

  • Moscoso, M., Domenech, M., & García, E. (2010). Vancomycin tolerance in clinical and laboratory Streptococcus pneumoniae isolates depends on reduced enzyme activity of the major LytA autolysin or cooperation between CiaH histidine kinase and capsular polysaccharide. Molecular Microbiology, 77, 1052–1064.

    CAS  Google Scholar 

  • Mrazek, J., Gaynon, L. H., & Karlin, S. (2002). Frequent oligonucleotide motifs in genomes of three Streptococci. Nucleic Acids Research, 30, 4216–4221.

    Article  PubMed  CAS  Google Scholar 

  • Murayama, K., Orth, P., de la Hoz, A. B., Alonso, J. C., & Saenger, W. (2001). Crystal structure of omega transcriptional repressor encoded by Streptococcus pyogenes plasmid pSM19035 at 1.5 A resolution. Journal of Molecular Biology, 314, 789–796.

    Article  PubMed  CAS  Google Scholar 

  • Mutschler, H., & Meinhart, A. (2011). ε/ζ systems: Their role in resistance, virulence, and their potential for antibiotic development. Journal of Molecular Medicine, 89, 1183–1194.

    Article  PubMed  CAS  Google Scholar 

  • Nieto, C., Cherny, I., Khoo, S. K., de García Lacoba, M., Chan, W. T., Yeo, C. C., et al. (2007). The yefM-yoeB toxin-antitoxin systems of Escherichia coli and Streptococcus pneumoniae: Functional and structural correlation. Journal of Bacteriology, 189, 1266–1278.

    Article  PubMed  CAS  Google Scholar 

  • Nieto, C., Pellicer, T., Balsa, D., Christensen, S. K., Gerdes, K., & Espinosa, M. (2006). The chromosomal relBE2 toxin-antitoxin locus of Streptococcus pneumoniae: Characterization and use of a bioluminescence resonance energy transfer assay to detect toxin-antitoxin interaction. Molecular Microbiology, 59, 1280–1296.

    Article  PubMed  CAS  Google Scholar 

  • Nieto, C., Sadowy, E., de la Campa, A. G., Hryniewicz, W., & Espinosa, M. (2010). The relBE2Spn toxin-antitoxin system of Streptococcus pneumoniae: Role in antibiotic tolerance and functional conservation in clinical isolates. PLoS ONE, 5, e11289.

    Article  PubMed  Google Scholar 

  • O’Brien, K. L., Wolfson, L. J., Watt, J. P., Henkle, E., Deloria-Knoll, M., McCall, N., et al. (2009). Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: Global estimates. Lancet, 374, 893–902.

    Article  PubMed  Google Scholar 

  • Olofsson, H., & Ripa, J. N. J. (2009). Bet-hedging as an evolutionary game: The trade-off between egg size and number. Proceedings of the Royal Society B, 276, 2963–2969.

    Article  PubMed  Google Scholar 

  • Overgaard, M., Borch, J., Jørgensen, M. G., & Gerdes, K. (2008). Messenger RNA interferase RelE controls relBE transcription by conditional cooperativity. Molecular Microbiology, 69, 841–857.

    Article  PubMed  CAS  Google Scholar 

  • Pabo, C. O., & Sauer, R. T. (1992). Transcription factors: Structural families and principles of DNA recognition. Annual Review of Biochemistry, 61, 1053–1095.

    Article  PubMed  CAS  Google Scholar 

  • Pandey, D. P., & Gerdes, K. (2005). Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Research, 33, 966–976.

    Article  PubMed  CAS  Google Scholar 

  • Park, I.H., Kim, K.-H., Andrade, A.L., Briles, D.E., McDaniel, L.S., Nahm, M.H. (2012). Nontypeable pneumococci can be divided into multiple cps types, including one type expressing the novel gene pspK. mBio, 3, e00035-00012.

    Google Scholar 

  • Pedersen, K., Christensen, K. S., & Gerdes, K. (2002). Rapid induction and reversal of a bacteriostatic conditions by controlled expression of toxins and antitoxins. Molecular Microbiology, 45, 501–510.

    Article  PubMed  CAS  Google Scholar 

  • Perez-Trallero, E., Marimón, J. M., Alonso, M., Ercibengoa, M., & García-Arenzana, J. M. (2012). Decline and rise of the antimicrobial susceptibility of Streptococcus pneumoniae isolated from middle ear fluid in children: Influence of changes in circulating serotypes. Antimicrobial Agents and Chemotherapy, 56, 3989–3991.

    Article  PubMed  CAS  Google Scholar 

  • Rao, C. V., Wolf, D. M., & Arkin, A. P. (2002). Control, exploitation and tolerance of intracellular noise. Nature, 420, 231–237.

    Article  PubMed  CAS  Google Scholar 

  • Rimini, R., Jansson, B., Feger, G., Roberts, T. C., de Francesco, M., Gozzi, A., et al. (2000). Global analysis of transcription kinetics during competence development in Streptococcus pneumoniae using high density DNA arrays. Molecular Microbiology, 36, 1279–1292.

    Article  PubMed  CAS  Google Scholar 

  • Saluja, S. K., & Weiser, J. N. (1995). The genetic basis of colony opacity in Streptococcus pneumoniae: Evidence for the effect of box elements on the frequency of phenotypic variation. Molecular Microbiology, 16, 215–227.

    Article  PubMed  CAS  Google Scholar 

  • Shao, Y., Harrison, E. M., Bi, D., Tai, C., He, X., Ou, H.-Y., et al. (2010). TADB: A web-based resource for Type 2 toxin–antitoxin loci in bacteria and archaea. Nucleic Acids Research, 39, D606–D611.

    Article  PubMed  Google Scholar 

  • Stocker, W., & Bode, W. (1995). Structural features of a superfamily of zinc-endopeptidases: The metzincins. Current Opinion in Structural Biology, 5, 383–390.

    Article  PubMed  CAS  Google Scholar 

  • Takagi, H., Kakuta, Y., Okada, T., Yao, M., Tanaka, I., & Kimura, M. (2005). Crystal structure of archaeal toxin-antitoxin RelE-RelB complex with implications for toxin activity and antitoxin effects. Nature Structural and Molecular Biology, 12, 327–331.

    Article  PubMed  CAS  Google Scholar 

  • Thattai, M., & van Oudenaarden, A. (2004). Stochastic gene expression in fluctuating environments. Genetics, 167, 523–530.

    Article  PubMed  Google Scholar 

  • Walker, J. A., Allen, R. L., Falmagne, P., Johnson, M. K., & Boulnois, G. J. (1987). Molecular cloning, characterization, and complete nucleotide sequence of the gene for pneumolysin, the sulfhydryl-activated toxin of Streptococcus pneumoniae. Infection and Immunity, 55, 1184–1189.

    PubMed  CAS  Google Scholar 

  • Zhang, Y., & Inouye, M. (2009). The inhibitory mechanism of protein synthesis by YoeB, an Escherichia coli toxin. Journal of Biological Chemistry, 284, 6627–6638.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Thanks are due to members of the INTERMODS Consortium for critical reading of the manuscript, and to members of Espinosa’s lab for many fruitful discussions. C. C. Y. would like to thank A. Meinhart, J. A. Harikrishna and past members of his lab for the productive work and discussions as well as the camaraderie. While this chapter was written, our labs were supported with grants from: the Spanish Ministry of Economy and Competitiveness (grants CSD-2008-00013, INTERMODS, and BFU2010-19597 to M.E.) and the Malaysian Ministry of Science, Technology and Innovation (grants 09-99-06-0104-EA001, 02-02-05-SF0019, 02-02-05-SF0026 and SAGA grant M18 to C.C.Y.)

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  1. Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, Ramiro de Maeztu 9, E28040, Madrid, Spain

    Wai Ting Chan, Inma Moreno-Córdoba & Manuel Espinosa

  2. Faculty of Agriculture and Biotechnology, Universiti Sultan Zainal Abidin, Jalan Sultan Mahmud, 20400, Kuala Terengganu, Malaysia

    Chew Chieng Yeo

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  1. Wai Ting Chan
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Correspondence to Manuel Espinosa .

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  1. Inst. for Cell and Molecular Bioscience, Centre for Bacterial Cell Biology, Newcastle University, Richardson Road, Newcastle upon Tyne, NE2 4AX, United Kingdom

    Kenn Gerdes

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Chan, W.T., Moreno-Córdoba, I., Yeo, C.C., Espinosa, M. (2013). Toxin-Antitoxin Loci in Streptococcus pneumoniae . In: Gerdes, K. (eds) Prokaryotic Toxin-Antitoxins. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-33253-1_18

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