Negative frequency-dependent selection and asymmetrical transformation stabilise multi-strain bacterial population structures
1.
Russell JB. Discussion on diphtheria. BMJ. 1891;2:631–40.
Article Google Scholar
2.
Joseph FH. Notes on some pathogenic bacteria as found in the Transvaal, and the variations from their European prototype. Rep. S Afr Assoc Adv Sci. 1904;2:237–42.
Google Scholar
3.
Eyre JW, Washbourn JW. Varities and virulence of the pneumococcus. Lancet. 1899;153:19–22.
Article Google Scholar
4.
Gladstone RA, Lo SW, Lees JA, Croucher NJ, van Tonder AJ, Corander J, et al. International genomic definition of pneumococcal lineages, to contextualise disease, antibiotic resistance and vaccine impact. EBioMedicine. 2019;43:338–46.
PubMed PubMed Central Article Google Scholar
5.
Colijn C, Corander J, Croucher NJ. Designing ecologically optimized pneumococcal vaccines using population genomics. Nat Microbiol. 2020;5:473–85.
CAS PubMed Article PubMed Central Google Scholar
6.
Weinberger DM, Malley R, Lipsitch M. Serotype replacement in disease after pneumococcal vaccination. Lancet. 2011;378:1962–73.
PubMed PubMed Central Article Google Scholar
7.
Lefevre JC, Faucon G, Sicard AM, Gasc AM. DNA fingerprinting of Streptococcus pneumoniae strains by pulsed-field gel electrophoresis. J Clin Microbiol. 1993;31:2724 LP–8.
Article Google Scholar
8.
Selander RK, Levin BR. Genetic diversity and structure in Escherichia coli populations. Science. 1980;210:545–7.
CAS PubMed Article PubMed Central Google Scholar
9.
Smith JM, Smith NH, O’Rourke M, Spratt BG. How clonal are bacteria? Proc Natl Acad Sci USA. 1993;90:4384–8.
CAS PubMed Article PubMed Central Google Scholar
10.
Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA. 1998;95:3140–5.
CAS PubMed Article PubMed Central Google Scholar
11.
Smith JM, Feil EJ, Smith NH. Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays. 2000;22:1115–22.
CAS PubMed Article PubMed Central Google Scholar
12.
Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, Hanage WP. Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat Commun. 2014;5:5471.
PubMed PubMed Central Article Google Scholar
13.
Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo S, Weiser JN, et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res. 2019;29:304–16.
CAS PubMed PubMed Central Article Google Scholar
14.
Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14:e1007261.
PubMed PubMed Central Article CAS Google Scholar
15.
Hanage WP, Spratt BG, Turner KME, Fraser C. Modelling bacterial speciation. Philos Trans R Soc B Biol Sci. 2006;361:2039–44.
Article Google Scholar
16.
Ford Doolittle W, Papke RT. Genomics and the bacterial species problem. Genome Biol. 2006;7:116.
PubMed Article CAS PubMed Central Google Scholar
17.
Shapiro BJ, David LA, Friedman J, Alm EJ. Looking for Darwin’s footprints in the microbial world. Trends Microbiol. 2009;17:196–204.
CAS PubMed Article PubMed Central Google Scholar
18.
Abu-Raddad LJ, Ferguson NM. The impact of cross-immunity, mutation and stochastic extinction on pathogen diversity. Proc R Soc B Biol Sci. 2004;271:2431–8.
Article Google Scholar
19.
Fraser C, Hanage WP, Spratt BG. Neutral microepidemic evolution of bacterial pathogens. Proc Natl Acad Sci USA. 2005;102:1968–73.
CAS PubMed Article PubMed Central Google Scholar
20.
Corander J, Fraser C, Gutmann MU, Arnold B, Hanage WP, Bentley SD, et al. Frequency-dependent selection in vaccine-associated pneumococcal population dynamics. Nat Ecol Evol. 2017;1:1950–60.
PubMed PubMed Central Article Google Scholar
21.
Buckee CO, Jolley KA, Recker M, Penman B, Kriz P, Gupta S, et al. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc Natl Acad Sci USA. 2008;105:15082–7.
CAS PubMed Article PubMed Central Google Scholar
22.
Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM, Parkhill J, et al. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet. 2013;45:656–63.
CAS PubMed PubMed Central Article Google Scholar
23.
Croucher NJ, Hanage WP, Harris SR, McGee L, van der Linden M, de Lencastre H, et al. Variable recombination dynamics during the emergence, transmission and ‘disarming’ of a multidrug-resistant pneumococcal clone. BMC Biol. 2014;12:49.
PubMed PubMed Central Article CAS Google Scholar
24.
Croucher NJ, Chewapreecha C, Hanage WP, Harris SR, McGee L, van der Linden M, et al. Evidence for soft selective sweeps in the evolution of pneumococcal multidrug resistance and vaccine escape. Genome Biol Evol. 2014;6:1589–602.
PubMed PubMed Central Article CAS Google Scholar
25.
Vos M. A species concept for bacteria based on adaptive divergence. Trends Microbiol. 2011;19:1–7.
CAS PubMed Article PubMed Central Google Scholar
26.
Whitaker RJ. Allopatric origins of microbial species. Philos Trans R Soc B Biol Sci. 2006;361:1975–84.
Article Google Scholar
27.
Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. The bacterial species challenge: Making sense of genetic and ecological diversity. Science. 2009;323:741–6.
CAS PubMed Article PubMed Central Google Scholar
28.
Hanage WP, Fraser C, Spratt BG. Fuzzy species among recombinogenic bacteria. BMC Biol. 2005;3:6.
PubMed PubMed Central Article CAS Google Scholar
29.
Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science. 2007;315:476–80.
CAS PubMed PubMed Central Article Google Scholar
30.
Sheppard SK, McCarthy ND, Falush D, Maiden MCJ. Convergence of Campylobacter species: implications for bacterial evolution. Science. 2008;320:237–9.
CAS PubMed Article PubMed Central Google Scholar
31.
Laible G, Spratt BG, Hakenbeck R. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin‐resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol. 1991;5:1993–2002.
CAS PubMed Article PubMed Central Google Scholar
32.
Dowson CG, Coffey TJ, Kell C, Whiley RA. Evolution of penicillin resistance in Streptococcus pneumoniae; the role of Streptococcus mitis in the formation of a low affinity PBP2B in S. pneumoniae. Mol Microbiol. 1993;9:635–43.
CAS PubMed Article PubMed Central Google Scholar
33.
Majewski J, Zawadzki P, Pickerill P, Cohan FM, Dowson CG. Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J Bacteriol. 2000;182:1016–23.
CAS PubMed PubMed Central Article Google Scholar
34.
Bobay L-M, Ochman H. Biological Species Are Universal across Life’s Domains. Genome Biol Evol. 2017;9:491–501.
PubMed Central Article Google Scholar
35.
Croucher NJ, Harris SR, Barquist L, Parkhill J, Bentley SD. A high-resolution view of genome-wide pneumococcal transformation. PLoS Pathog. 2012;8:e1002745.
CAS PubMed PubMed Central Article Google Scholar
36.
Cohan F. Bacterial species and speciation. Syst Biol. 2001;50:513–24.
CAS PubMed Article PubMed Central Google Scholar
37.
Nosil P, Funk DJ, Ortiz-Barrientos D. Divergent selection and heterogeneous genomic divergence. Mol Ecol. 2009;18:375–402.
PubMed Article PubMed Central Google Scholar
38.
Cohan FM, Perry EB. A systematics for discovering the fundamental units of bacterial diversity. Curr Biol. 2007;17:R373–R386.
CAS PubMed Article PubMed Central Google Scholar
39.
Marttinen P, Hanage WP. Speciation trajectories in recombining bacterial species. PLoS Comput Biol. 2017;13:e1005640.
PubMed PubMed Central Article CAS Google Scholar
40.
Gjini E, Valente C, Sá-Leão R, Gomes MGM. How direct competition shapes coexistence and vaccine effects in multi-strain pathogen systems. J Theor Biol. 2016;388:50–60.
PubMed Article PubMed Central Google Scholar
41.
Numminen E, Cheng L, Gyllenberg M, Corander J. Estimating the transmission dynamics of Streptococcus pneumoniae from strain prevalence data. Biometrics. 2013;69:748–57.
PubMed Article PubMed Central Google Scholar
42.
Majewski J, Cohan FM. Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics. 1999;152:1459–74.
CAS PubMed PubMed Central Google Scholar
43.
Wiedenbeck J, Cohan FM. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev. 2011;35:957–76.
CAS PubMed Article PubMed Central Google Scholar
44.
Barraclough TG, Balbi KJ, Ellis RJ. Evolving concepts of bacterial species. Evol Biol. 2012;39:148–57.
Article Google Scholar
45.
Chesson P. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst. 2000;31:343–66.
Article Google Scholar
46.
Neher RA, Shraiman BI. Competition between recombination and epistasis can cause a transition from allele to genotype selection. Proc Natl Acad Sci USA. 2009;106:6866–71.
CAS PubMed Article PubMed Central Google Scholar
47.
Mostowy R, Croucher NJ, Andam CP, Corander J, Hanage WP, Marttinen P. Efficient inference of recent and ancestral recombination within bacterial populations. Mol Biol Evol. 2017;34:1167–82.
CAS PubMed PubMed Central Article Google Scholar
48.
Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, et al. Rapid pneumococcal evolution in response to clinical interventions. Science. 2011;331:430–4.
CAS PubMed PubMed Central Article Google Scholar
49.
Romero P, Croucher NJ, Hiller NL, Hu FZ, Ehrlich GD, Bentley SD, et al. Comparative genomic analysis of ten Streptococcus pneumoniae temperate bacteriophages. J Bacteriol. 2009;191:4854–62.
CAS PubMed PubMed Central Article Google Scholar
50.
Ferguson NM, Galvanl AP, Bush RM. Ecological and immunological determinants of influenza evolution. Nature. 2003;422:428–33.
CAS PubMed Article PubMed Central Google Scholar
51.
Cobey S, Lipsitch M. Niche and neutral effects of acquired immunity permit coexistence of pneumococcal serotypes. Science. 2012;335:1376–80.
CAS PubMed PubMed Central Article Google Scholar
52.
Cobey S. Pathogen evolution and the immunological niche. Ann N Y Acad Sci. 2014;1320:1–15.
CAS PubMed PubMed Central Article Google Scholar
53.
Levin BR. Frequency-dependent selection in bacterial populations. Philos Trans R Soc Lond B Biol Sci. 1988;319:459–72.
CAS PubMed Article PubMed Central Google Scholar
54.
Gomes MGM, Medley GF, Nokes DJ. On the determinants of population structure in antigenically diverse pathogens. Proc R Soc Lond Ser B Biol Sci. 2002;269:227–33.
Article Google Scholar
55.
Binsker U, Lees JA, Hammond AJ, Weiser JN. Immune exclusion by naturally acquired secretory IgA against pneumococcal pilus-1. J Clin Investig. 2020;130:927–41.
CAS PubMed Article PubMed Central Google Scholar
56.
Gupta S, Maiden MCJ, Feavers IM, Nee S, May RM, Anderson RM. The maintenance of strain structure in populations of recombining infectious agents. Nat Med. 1996;2:437–42.
CAS PubMed Article PubMed Central Google Scholar
57.
Gupta S, Ferguson N, Anderson R. Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. Science. 1998;280:912–5.
CAS PubMed Article PubMed Central Google Scholar
58.
Croucher NJ, Campo JJ, Le TQ, Liang X, Bentley SD, Hanage WP, et al. Diverse evolutionary patterns of pneumococcal antigens identified by pangenome-wide immunological screening. Proc Natl Acad Sci USA. 2017;114:E357–66.
CAS PubMed Article PubMed Central Google Scholar
59.
Weinberger DM, Dagan R, Givon‐Lavi N, Regev‐Yochay G, Malley R, Lipsitch M. Epidemiologic evidence for serotype‐specific acquired immunity to pneumococcal carriage. J Infect Dis. 2008;197:1511–8.
PubMed Article PubMed Central Google Scholar
60.
Malley R, Lipsitch M, Bogaert D, Thompson CM, Hermans P, Claire Watkins A, et al. Serum antipneumococcal antibodies and pneumococcal colonization in adults with chronic obstructive pulmonary disease. J Infect Dis. 2007;196:928–35.
PubMed Article Google Scholar
61.
Campo JJ, Le TQ, Pablo JV, Hung C, Teng AA, Tettelin H, et al. Panproteome-wide analysis of antibody responses to whole cell pneumococcal vaccination. Elife. 2018;7:e37015.
PubMed PubMed Central Article Google Scholar
62.
Buckee CO, Koelle K, Mustard MJ, Gupta S. The effects of host contact network structure on pathogen diversity and strain structure. Proc Natl Acad Sci USA. 2004;101:10839 LP–44.
Article Google Scholar
63.
Buckee CO, Recker M, Watkins ER, Gupta S. Role of stochastic processes in maintaining discrete strain structure in antigenically diverse pathogen populations. Proc Natl Acad Sci USA. 2011;108:15504 LP–9.
Article Google Scholar
64.
Watkins ER, Penman BS, Lourenço J, Buckee CO, Martin C, Maiden MCJ, et al. Vaccination drives changes in metabolic and virulence profiles of Streptococcus pneumoniae. PLoS Pathog. 2015;11:e1005034.
PubMed PubMed Central Article CAS Google Scholar
65.
Skwark MJ, Croucher NJ, Puranen S, Chewapreecha C, Pesonen M, Xu YY, et al. Interacting networks of resistance, virulence and core machinery genes identified by genome-wide epistasis analysis. PLoS Genet. 2017;13:e1006508.
PubMed PubMed Central Article CAS Google Scholar
66.
Pensar J, Puranen S, Arnold B, MacAlasdair N, Kuronen J, Tonkin-Hill G, et al. Genome-wide epistasis and co-selection study using mutual information. Nucleic Acids Res. 2019;47:e112.
CAS PubMed PubMed Central Article Google Scholar
67.
Rocha EPC. Neutral theory, microbial practice: challenges in bacterial population genetics. Mol Biol Evol. 2018;35:1338–47.
CAS PubMed Article PubMed Central Google Scholar
68.
Azarian T, Martinez PPP, Arnold BJ, Grant LR, Corander J, Fraser C, et al. Frequency-dependent selection can forecast evolution in Streptococcus pneumoniae. PLoS Biol. 2020;18:e3000878.
CAS PubMed PubMed Central Article Google Scholar
69.
Johnston C, Campo N, Bergé MJ, Polard P, Claverys JP. Streptococcus pneumoniae, le transformiste. Trends Microbiol. 2014;22:113–9.
CAS PubMed Article PubMed Central Google Scholar
70.
Marttinen P, Gutmann MU, Croucher NJ, Corander J, Hanage WP. Recombination produces coherent bacterial species clusters in both core and accessory genomes. Micro Genom. 2015;1:e000038.
Google Scholar
71.
Croucher NJ, Mostowy R, Wymant C, Turner P, Bentley SD, Fraser C. Horizontal DNA Transfer mechanisms of bacteria as weapons of intragenomic conflict. PLoS Biol. 2016;14:e1002394.
PubMed PubMed Central Article CAS Google Scholar
72.
Apagyi KJ, Fraser C, Croucher NJ. Transformation asymmetry and the evolution of the bacterial accessory genome. Mol Biol Evol. 2018;35:575–81.
CAS PubMed Article PubMed Central Google Scholar
73.
Spearman C. The proof and measurement of association between two things. Am J Psychol. 1904;100:441–71.
Article Google Scholar
74.
Smirnov N. Table for estimating the goodness of fit of empirical distributions. Ann Math Stat. 1948;19:279–81.
Article Google Scholar
75.
Kelley T. Statistical method. New York: Macmillan; 1923.
Google Scholar
76.
Simpson EH. Measurement of diversity. Nature. 1949;163:688.
Article Google Scholar
77.
Kimura M. On the probability of fixation of mutant genes in a population. Genetics. 1962;47:713–9.
CAS PubMed PubMed Central Google Scholar
78.
Hanage WP, Fraser C, Spratt BG. The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol. 2006;239:210–9.
CAS PubMed Article PubMed Central Google Scholar
79.
Lawrence JG. Gene transfer in bacteria: speciation without species? Theor Popul Biol. 2002;61:449–60.
PubMed Article PubMed Central Google Scholar
80.
Pybus OG, Harvey PH. Testing macro-evolutionary models using incomplete molecular phylogenies. Proc R Soc B Biol Sci. 2000;267:2267–72.
CAS Article Google Scholar
81.
Barraclough TG, Birky CW, Burt A. Diversification in sexual and asexual organisms. Evolution. 2003;57:2166–72.
PubMed Article PubMed Central Google Scholar
82.
Hudson RR. Gene genealogies and the coalescent process. In: Oxford surveys in evolutionary biology. Oxford: Oxford University Press; 1990. p. 1–44.
83.
Numminen E, Gutmann M, Shubin M, Marttinen P, Méric G, van Schaik W, et al. The impact of host metapopulation structure on the population genetics of colonizing bacteria. J Theor Biol. 2016;396:53–62.
PubMed Article PubMed Central Google Scholar
84.
Castillo-Chavez C, Hethcote HW, Andreasen V, Levin SA, Liu WM. Epidemiological models with age structure, proportionate mixing, and cross-immunity. J Math Biol. 1989;27:233–58.
CAS PubMed Article PubMed Central Google Scholar
85.
McNally A, Kallonen T, Connor C, Abudahab K, Aanensen D, Horner C, et al. Signatures of negative frequency dependent selection in colonisation factors and the evolution of a multi-drug resistant lineage of Escherichia coli. MBio. 2019;10:e00644–19.
CAS PubMed PubMed Central Article Google Scholar
86.
Kwun MJ, Oggioni MR, Bentley SD, Fraser C, Croucher NJ. Synergistic activity of mobile genetic element defences in Streptococcus pneumoniae. Genes. 2019;10:707.
CAS PubMed Central Article Google Scholar
87.
Iranzo J, Puigbo P, Lobkovsky AE, Wolf YI, Koonin EV. Inevitability of genetic parasites. Genome Biol Evol. 2016;8:2856–69. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5631039/.
CAS PubMed PubMed Central Article Google Scholar
88.
Budroni S, Siena E, Dunning Hotopp JC, Seib KL, Serruto D, Nofroni C, et al. Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination. Proc Natl Acad Sci USA. 2011;108:4494–9.
CAS PubMed Article PubMed Central Google Scholar
89.
Johnston C, Martin B, Granadel C, Polard P, Claverys JP. Programmed protection of foreign DNA from restriction allows pathogenicity island exchange during pneumococcal transformation. PLoS Pathog. 2013;9:e1003178.
CAS PubMed PubMed Central Article Google Scholar
90.
Kwun MJ, Oggioni MR, De Ste Croix M, Bentley SD, Croucher NJ. Excision-reintegration at a pneumococcal phase-variable restriction-modification locus drives within- and between-strain epigenetic differentiation and inhibits gene acquisition. Nucleic Acids Res. 2018;46:11438–53.
CAS PubMed PubMed Central Google Scholar More