Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Lourenço, José ^a   Watkins, Eleanor R ^a   Obolski, Uri ^a   Peacock, Samuel J ^a   Morris, Callum ^b   Maiden, Martin C J ^a   Gupta, Sunetra ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONIN 60;

BACTERIAL CAPSULE; EPISTASIS; EVOLUTION; GENETICS; IMMUNOLOGY; MACHINE LEARNING; OPERON; SEROTYPING; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL CAPSULES; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CHAPERONIN 60; EPISTASIS, GENETIC; MACHINE LEARNING; OPERON; SEROTYPING; STREPTOCOCCUS PNEUMONIAE;

EID: 85028031491     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-08990-z     Document Type: Article

References (88)

1. Song, J. Y. et al. Clinical and economic burden of invasive pneumococcal disease in adults: a multicenter hospital-based study. BMC infectious diseases 13, 202 (2013).
2. O'Brien, K. L. et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. The Lancet 374, 893-902 (2009).
3. Hausdorff, W. P., Feikin, D. R. & Klugman, K. P. Epidemiological differences among pneumococcal serotypes. Lancet Infectious Diseases 5, 83-93 (2005).
4. Cobey, S. & Lipsitch, M. Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science (New York, N.Y.) 335, 1376-80 (2012).
5. Maiden, M. C. et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences of the United States of America 95, 3140-5 (1998).
6. Spratt, B. G. Multilocus sequence typing: Molecular typing of bacterial pathogens in an era of rapid DNA sequencing and the Internet. Current Opinion in Microbiology 2, 312-316 (1999).
7. Croucher, N. J. et al. Diversification of bacterial genome content through distinct mechanisms over different timescales. Nature Communications 5, 1-12 (2014).
8. Croucher, N. J. et al. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nature genetics 45, 656-63 (2013).
9. Cremers, A. J. H. et al. The post-vaccine microevolution of invasive Streptococcus pneumoniae. Scientific reports 5, 14952 (2015).
10. Brueggemann, A. B. et al. Clonal Relationships between Invasive and Carriage Streptococcus Pneumoniae and Serotype-and Clone-Specific Differences in Invasive Disease Potential. The Journal of Infectious Diseases 187, 1424-1432 (2003).
11. Beall, B. W. et al. Shifting genetic structure of invasive serotype 19A pneumococci in the United States. Journal of Infectious Diseases 203, 1360-1368 (2011).
12. Henriques-Normark, B., Blomberg, C., Dagerhamn, J., Bättig, P. & Normark, S. The rise and fall of bacterial clones: Streptococcus pneumoniae. Nature reviews. Microbiology 6, 827-37 (2008).
13. Fraser, C., Hanage, W. P. & Spratt, B. G. Neutral microepidemic evolution of bacterial pathogens. Proceedings of the National Academy of Sciences of the United States of America 102, 1968-73 (2005).
14. Buckee, C. O. et al. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proceedings of the National Academy of Sciences of the United States of America 105, 15082-7 (2008).
15. Watkins, E. R., Maiden, M. C. & Gupta, S. Metabolic competition as a driver of bacterial population structure. Future Microbiology fmb-2016-0079 (2016).
16. Bidossi, A. et al. A functional genomics approach to establish the complement of carbohydrate transporters in Streptococcus pneumoniae. PLoS ONE 7, e33320 (2012).
17. Watkins, E. R. et al. Vaccination Drives Changes in Metabolic and Virulence Profiles of Streptococcus pneumoniae. PLoS pathogens 11, e1005034 (2015).
18. Meng, Y. A., Yu, Y., Cupples, L. A., Farrer, L. A. & Lunetta, K. L. Performance of random forest when SNPs are in linkage disequilibrium. BMC Bioinformatics 10, 78 (2009).
19. Slabbinck, B., Waegeman, W., Dawyndt, P., De Vos, P. & De Baets, B. From learning taxonomies to phylogenetic learning: integration of 16S rRNA gene data into FAME-based bacterial classification. BMC bioinformatics 11, 69 (2010).
20. Aguas, R. & Ferguson, N. M. Feature Selection Methods for Identifying Genetic Determinants of Host Species in RNA Viruses. PLoS Computational Biology 9 (2013).
21. Eng, C. L. P., Tong, J. C. & Tan, T. W. Predicting host tropism of influenza A virus proteins using random forest. BMC Medical Genomics 7, S1-S1 (2014).
22. Eng, C. L. P., Tong, J. C. & Tan, T. W. Distinct host tropism protein signatures to identify possible zoonotic influenza a viruses. PLoS ONE 11, 1-12 (2016).
23. Lupolova, N., Dallman, T. J., Matthews, L., Bono, J. L. & Gally, D. L. Support vector machine applied to predict the zoonotic potential of E. coli O157 cattle isolates. Proceedings of the National Academy of Sciences 201606567 (2016).
24. Alam, M. T. et al. Dissecting vancomycin-intermediate resistance in staphylococcus aureus using genome-wide association. Genome Biology and Evolution 6, 1174-1185 (2014).
25. Burstein, D. et al. Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires. Nature Genetics 48, 167-175 (2016).
26. Klemm, E. & Dougan, G. Advances in Understanding Bacterial Pathogenesis Gained from Whole-Genome Sequencing and Phylogenetics. Cell Host and Microbe 19, 599-610 (2016).
27. Austerlitz, F. et al. DNA barcode analysis: a comparison of phylogenetic and statistical classification methods. BMC bioinformatics 10(Suppl 1), S10 (2009).
28. Bentley, S. D. et al. Putatively novel serotypes and the potential for reduced vaccine effectiveness: capsular locus diversity revealed among 5,405 pneumococcal genomes. Microbial Genomics 2 (2016).
29. Glazunova, O. O., Raoult, D. & Roux, V. Partial sequence comparison of the rpoB, sodA, groEL and gyrB genes within the genus Streptococcus. International Journal of Systematic and Evolutionary Microbiology 59, 2317-2322 (2009).
30. Teng, L.-j. et al. groESL Sequence Determination, Phylogenetic Analysis, and Species Differentiation for Viridans Group Streptococci groESL Sequence Determination, Phylogenetic Analysis, and Species Differentiation for Viridans Group Streptococci. Journal of Clinical Microbiology 40, 3172-3178 (2002).
31. Hung, W. C., Tsai, J. C., Hsueh, P. R., Chia, J. S. & Teng, L. J. Species identification of mutans streptococci by groESL gene sequence. Journal of Medical Microbiology 54, 857-862 (2005).
32. Obregón, V. et al. Molecular peculiarities of the lytA gene isolated from clinical pneumococcal strains that are bile insoluble. Journal of Clinical Microbiology 40, 2545-2554 (2002).
33. Arbique, J. C. et al. Accuracy of phenotypic and genotypic testing for identification of Streptococcus pneumoniae and description of Streptococcus pseudopneumoniae sp. nov. Journal of Clinical Microbiology 42, 4686-4696 (2004).
34. Poyart, C., Quesne, G., Coulon, S., Berche, P. & Trieu-Cuot, P. Identification of streptococci to species level by sequencing the gene encoding the manganese-dependent superoxide dismutase. Journal of Clinical Microbiology 36, 41-47 (1998).
35. Martín-Galiano, A. J., Balsalobre, L., Fenoll, A. & De la Campa, A. G. Genetic characterization of optochin-susceptible viridans group streptococci. Antimicrobial Agents and Chemotherapy 47, 3187-3194 (2003).
36. Spellerberg, B. et al. Lmb, a protein with similarities to the LraI adhesin family, mediates attachment of Streptococcus agalactiae to human laminin. Infection and Immunity 67, 871-878 (1999).
37. Terao, Y., Kawabata, S., Kunitomo, E., Nakagawa, I. & Hamada, S. Novel laminin-binding protein of Streptococcus pyogenes, Lbp, is involved in adhesion to epithelial cells. Infection and Immunity 70, 993-997 (2002).
38. Zhang, Y. M. et al. Prevalent distribution and conservation of streptococcus suis lmb protein and its protective capacity against the chinese highly virulent strain infection. Microbiological Research 169, 395-401 (2014).
39. Wahid, R. M. et al. Immune response to a laminin-binding protein (Lmb) in group a streptococcal infection. Pediatrics International 47, 196-202 (2005).
40. Jomaa, M. et al. Immunization with the iron uptake ABC transporter proteins PiaA and PiuA prevents respiratory infection with Streptococcus pneumoniae. Vaccine 24, 5133-5139 (2006).
41. Reizer, J., Reizer, A. & Saier, M. H. A functional superfamily of sodium/solute symporters. Biochimica et biophysica acta 1197, 133-66 (1994).
42. Wilding, E. I. et al. Identification, essentiality and evolution of the mevalonate pathway for isopentenyl diphosphate biosynthesis in {Gram}-positive cocci. J. Bacteriology 182, 4319-4327 (2000).
43. Buhaescu, I. & Izzedine, H. Mevalonate pathway: A review of clinical and therapeutical implications. Clinical Biochemistry 40, 575-584 (2007).
44. Holstein, S. A. & Hohl, R. J. Isoprenoids: Remarkable diversity of form and function. Lipids 39, 293-309 (2004).
45. Boyle-Vavra, S., Yin, S., Jo, D. S., Montgomery, C. P. & Daum, R. S. VraT/YvqF is required for methicillin resistance and activation of the VraSR regulon in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 57, 83-95 (2013).
46. Garvey, M. I., Baylay, A. J., Wong, R. L. & Piddock, L. J. V. Overexpression of patA and patB, which encode ABC transporters, is associated with fluoroquinolone resistance in clinical isolates of Streptococcus pneumoniae. Antimicrobial Agents and Chemotherapy 55, 190-196 (2011).
47. El Garch, F. et al. Fluoroquinolones induce the expression of patA and patB, which encode ABC efflux pumps in Streptococcus pneumoniae. Journal of Antimicrobial Chemotherapy 65, 2076-2082 (2010).
48. Boncoeur, E. et al. PatA and PatB form a functional heterodimeric ABC multidrug efflux transporter responsible for the resistance of streptococcus pneumoniae to fluoroquinolones. Biochemistry 51, 7755-7765 (2012).
49. Joyce, E. A. et al. LuxS Is Required for Persistent Pneumococcal Carriage and Expression of Virulence and Biosynthesis Genes. Infection and Immunity 72, 2964-2975 (2004).
50. Xu, L. et al. Role of the luxS Quorum-Sensing System in Biofilm Formation and Virulence of Staphylococcus epidermidis Role of the luxS Quorum-Sensing System in Biofilm Formation and Virulence of Staphylococcus epidermidis. Infection and immunity 74, 488-496 (2006).
51. De Saizieu, A. et al. Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. Journal of Bacteriology 182, 4696-4703 (2000).
52. Reichmann, P. & Hakenbeck, R. Allelic variation in a peptide-inducible two-component system of Streptococcus pneumoniae. FEMS Microbiology Letters 190, 231-236 (2000).
53. Moye, Z. D., Burne, R. A. & Zeng, L. Uptake and metabolism of N-acetylglucosamine and glucosamine by Streptococcus mutans. Applied and Environmental Microbiology 80, 5053-5067 (2014).
54. García, P., González, M. P., García, E., García, J. L. & López, R. The molecular characterization of the first autolytic lysozyme of Streptococcus pneumoniae reveals evolutionary mobile domains. Molecular Microbiology 33, 128-138 (1999).
55. Eldholm, V., Johnsborg, O., Haugen, K., Ohnstad, H. S. & Havastein, L. S. Fratricide in Streptococcus pneumoniae: Contributions and role of the cell wall hydrolases CbpD, LytA and LytC. Microbiology 155, 2223-2234 (2009).
56. Iacobone, M., Mantero, F., Basso, S. M., Lumachi, F. & Favia, G. Results and long-term follow-up after unilateral adrenalectomy for ACTH-independent hypercortisolism in a series of fifty patients. Journal of Endocrinological Investigation 28, 327-332 (2005).
57. Pancholi, V. & Chhatwal, G. S. Housekeeping enzymes as virulence factors for pathogens. International Journal of Medical Microbiology 293, 391-401 (2003).
58. Humphries, H. E. & High, N. J. The role of licA phase variation in the pathogenesis of invasive disease by Haemophilus influenzae type b. FEMS Immunology and Medical Microbiology 34, 221-230 (2002).
59. Paterson, G. K., Nieminen, L., Jefferies, J. M. C. & Mitchell, T. J. PclA, a pneumococcal collagen-like protein with selected strain distribution, contributes to adherence and invasion of host cells. FEMS Microbiology Letters 285, 170-176 (2008).
60. Kim, S. N., Kim, S. W., Pyo, S. N. & Rhee, D. K. Molecular cloning and characterization of groESL operon in Streptococcus pneumoniae. Mol Cells 11, 360-368 (2001).
61. Cao, J. et al. Protection against pneumococcal infection elicited by immunization with multiple pneumococcal heat shock proteins. Vaccine 31, 3564-3571 (2013).
62. Péchiné, S., Hennequin, C., Boursier, C., Hoys, S. & Collignon, A. Immunization using GroEL decreases Clostridium difficile intestinal colonization. PLoS ONE 8 (2013).
63. Svenson, S. B. & Lindberg, A. L. F. A. Artificial Salmonella Vaccines: Salmonella typhimurium 0-Antigen-Specific Oligosaccharide-Protein Conjugates Elicit Protective Antibodies in Rabbits and Mice. Immunity and infection 32, 490-496 (1981).
64. Kalynych, S., Morona, R. & Cygler, M. Progress in understanding the assembly process of bacterial O-antigen. FEMS Microbiology Reviews 38, 1048-1065 (2014).
65. Serino, L. & Virji, M. Phosphorylcholine decoration of lipopolysaccharide differentiates commensal Neisseriae from pathogenic strains: Identification of licA-type genes in commensal Neisseriae. Molecular Microbiology 35, 1550-1559 (2000).
66. McInerney, J. O. More than tree dimensions: Inter-lineage evolution's ecological importance. Trends in Ecology and Evolution 28, 924-625 (2013).
67. Enright, M. C. & Spratt, B. G. Extensive variation in the ddl gene of penicillin-resistant Streptococcus pneumoniae results from a hitchhiking effect driven by the penicillin-binding protein 2b gene. Molecular biology and evolution 16, 1687-95 (1999).
68. Hayer-Hartl, M., Bracher, A. & Hartl, F. U. The GroEL-GroES Chaperonin Machine: A Nano-Cage for Protein Folding (2016).
69. Kerner, M. J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005).
70. Khan, M. N., Shukla, D., Bansal, A., Mustoori, S. & Ilavazhagan, G. Immunogenicity and protective efficacy of GroEL (hsp60) of Streptococcus pneumoniae against lethal infection in mice. FEMS Immunology and Medical Microbiology 56, 56-62 (2009).
71. Hennequin, C. et al. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 147, 87-96 (2001).
72. Wuppermann, F. N., Mölleken, K., Julien, M., Jantos, C. A. & Hegemann, J. H. Chlamydia pneumoniae GroEL1 protein is cell surface associated and required for infection of HEp-2 cells. Journal of Bacteriology 190, 3757-3767 (2008).
73. Chang, Q. et al. Stability of the pneumococcal population structure in Massachusetts as PCV13 was introduced. BMC infectious diseases 15, 68 (2015).
74. Croucher, N. J. et al. Selective and Genetic Constraints on Pneumococcal Serotype Switching. PLoS Genetics 11, 1-21 (2015).
75. Gupta, S. Chaos, Persistence, and Evolution of Strain Structure in Antigenically Diverse Infectious Agents. Science 280, 912-915 (1998).
76. Gupta, S. et al. The maintenance of strain structure in populations of recombining infectious agents. Nature medicine 2, 437-42 (1996).
77. Lourenço, J., Wikramaratna, P. S. & Gupta, S. MANTIS: an R package that simulates multilocus models of pathogen evolution. BMC bioinformatics 16, 176 (2015).
78. Bergé, M., Mortier-Barrière, I., Martin, B. & Claverys, J. P. Transformation of Streptococcus pneumoniae relies on DprA-and RecA-dependent protection of incoming DNA single strands. Molecular Microbiology 50, 527-536 (2003).
79. Venkatesh, R. et al. RecX protein abrogates ATP hydrolysis and strand exchange promoted by RecA: insights into negative regulation of homologous recombination. Proceedings of the National Academy of Sciences of the United States of America 99, 12091-12096 (2002).
80. Stohl, E. A. et al. Escherichia coli RecX inhibits RecA recombinase and coprotease activities in vitro and in vivo. Journal of Biological Chemistry 278, 2278-2285 (2003).
81. Galvão, C. W. et al. The RecX protein interacts with the RecA protein and modulates its activity in herbaspirillum seropedicae. Brazilian Journal of Medical and Biological Research 45, 1127-1134 (2012).
82. Jeltsch, A. Maintenance of species identity and controlling speciation of bacteria: A new function for restriction/modification systems Gene 317, 13-16 (2003).
83. Budroni, S. et al. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proceedings of the National Academy of Sciences of the United States of America 108, 4494-9 (2011).
84. Shah, R. et al. Replacement of GroEL in Escherichia coli by the Group II Chaperonin from the Archaeon Methanococcus maripaludis. Journal of Bacteriology 198, 2692-2700 (2016).
85. Altschul, S., Gish, W., Miller, W., Myers, E. & Lipman, D. Basic local alignment search tool. Journal of Molecular Biology 215, 403-410 (1990).
86. Breiman, L. Random forests. Machine Learning 45, 5-32 (2001).
87. Friedman, J., Hastie, T. J. & Tibshirani, R. The Elements of Statistical Learning. Springer Series in Statistics (Springer New York, New York, NY, 2001).
88. Liaw, a & Wiener, M. Classification and Regression by randomForest. R news 2, 18-22 (2002).