Population genetics and evolution of the pan-genome of Streptococcus pneumoniae

Novartis Vaccines and Diagnostics, Via Fiorentina 1, 53100 Siena, Italy.
International journal of medical microbiology: IJMM (Impact Factor: 3.61). 12/2011; 301(8):619-22. DOI: 10.1016/j.ijmm.2011.09.008
Source: PubMed


The genetic variability in bacterial species is much larger than in other kingdoms of life. The gene content between pairs of isolates can diverge by as much as 30% in species like Escherichia coli or Streptococcus pneumoniae. This unexpected finding led to the introduction of the concept of the pan-genome, the set of genes that can be found in a given bacterial species. The genome of any isolate is thus composed by a "core genome" shared by all strains and characteristic of the species, and a "dispensable genome" that accounts for many of the phenotypic differences between strains. The pan-genome is usually much larger than the genome of any single isolate and, given the ability of many bacteria to exchange genetic material with the environment, constitutes a reservoir that could enhance their ability to survive in a mutating environment. To understand the evolution of the pan-genome of an important pathogen and its interactions with the commensal microbial flora, we have analyzed the genomes of 44 strains of Streptococcus pneumoniae, one of the most important causes of microbial diseases in humans. Despite evidence of extensive homologous recombination, the S. pneumoniae phylogenetic tree reconstructed from polymorphisms in the core genome identified major groups of genetically related strains. With the exception of serotype 1, the tree correlated poorly with capsular serotype, geographical site of isolation and disease outcome. The distribution of dispensable genes was consistent with phylogeny, although horizontal gene transfer events attenuated this correlation in the case of ancient lineages. Homologous recombination, involving short stretches of DNA, was the dominant evolutionary process of the core genome of S. pneumoniae. Genetic exchange with related species sharing the same ecological niche was the main mechanism of evolution of S. pneumonia; and S. mitis was the main reservoir of genetic diversity of S. pneumoniae. The pan-genome of S. pneumoniae increased logarithmically with the number of strains and linearly with the variability of the sample, suggesting that acquired genes accumulate proportionately to the age of clones.

34 Reads
  • Source
    • "The ability of the pneumococcus to donate and receive genetic material is not restricted to its own species. Novel genes can be acquired from other taxa, many of which also inhabit the same mucosal surfaces of the oral cavity and nasopharynx as the pneumococcus , indicating that a shared habitat can greatly facilitate inter-species mobilization of genes (Muzzi and Donati, 2011). Horizontal gene transfer (HGT) that traverses boundaries of traditionally named species can enhance the pneumococcal gene pool and lead to exceptionally variable genomes of individual isolates. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The genus Streptococcus contains 104 recognized species, many of which are associated with human or animal hosts. A globally prevalent human pathogen in this group is Streptococcus pneumoniae (the pneumococcus). While being a common resident of the upper respiratory tract, it is also a major cause of otitis media, pneumonia, bacteremia and meningitis, accounting for a high burden of morbidity and mortality worldwide. Recent findings demonstrate the importance of recombination and selection in driving the population dynamics and evolution of different pneumococcal lineages, allowing them to successfully evade the impacts of selective pressures such as vaccination and antibiotic treatment. We highlight the ability of pneumococci to respond to these pressures through processes including serotype replacement, capsular switching and horizontal gene transfer (HGT) of antibiotic resistance genes. The challenge in controlling this pathogen also lies in the exceptional genetic and phenotypic variation among different pneumococcal lineages, particularly in terms of their pathogenicity and resistance to current therapeutic strategies. The widespread use of pneumococcal conjugate vaccines, which target only a small subset of the more than 90 pneumococcal serotypes, provides us with a unique opportunity to elucidate how the processes of selection and recombination interact to generate a remarkable level of plasticity and heterogeneity in the pneumococcal genome. These processes also play an important role in the emergence and spread of multi-resistant strains, which continues to pose a challenge in disease control and/or eradication. The application of population of genomic approaches at different spatial and temporal scales will help improve strategies to control this global pathogen, and potentially other pathogenic streptococci.
    Infection Genetics and Evolution 11/2014; 61. DOI:10.1016/j.meegid.2014.11.007 · 3.02 Impact Factor
  • Source
    • "The study of the diversity among strains promotes our understanding of gene rearrangement, genomic plasticity as loss and gains and inversions in the genome. In addition, this research provides valuable information regarding molecular epidemiology, microevolution, lineage-specific genes and common genes among the isolates [6], contributing to the development of new therapies that are more effective for the control of caseous lymphadenitis (CLA). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Since the first successful attempt at sequencing the Corynebacterium pseudotuberculosis genome, large amounts of genomic, transcriptomic and proteomic data have been generated. C. pseudotuberculosis is an interesting bacterium due to its great zoonotic potential and because it causes considerable economic losses worldwide. Furthermore, different strains of C. pseudotuberculosis are capable of causing various diseases in different hosts. Currently, we seek information about the phylogenetic relationships between different strains of C. pseudotuberculosis isolates from different hosts across the world and to employ these data to develop tools to diagnose and eradicate the diseases these strains cause. In this review, we present the latest findings on C. pseudotuberculosis that have been obtained with the most advanced techniques for sequencing and genomic organization. We also discuss the development of in silico tools for processing these data to prompt a better understanding of this pathogen.
    Computational and Structural Biotechnology Journal 03/2013; 6(7):e201303013. DOI:10.5936/csbj.201303013
  • Source
    • "2012 ; Li et al . 2010 ; Muzzi and Donati 2011 "
    [Show abstract] [Hide abstract]
    ABSTRACT: Since the turn of the century the complete genome sequence of just one mouse strain, C57BL/6J, has been available. Knowing the sequence of this strain has enabled large-scale forward genetic screens to be performed, the creation of an almost complete set of embryonic stem (ES) cell lines with targeted alleles for protein-coding genes, and the generation of a rich catalog of mouse genomic variation. However, many experiments that use other common laboratory mouse strains have been hindered by a lack of whole-genome sequence data for these strains. The last 5 years has witnessed a revolution in DNA sequencing technologies. Recently, these technologies have been used to expand the repertoire of fully sequenced mouse genomes. In this article we review the main findings of these studies and discuss how the sequence of mouse genomes is helping pave the way from sequence to phenotype. Finally, we discuss the prospects for using de novo assembly techniques to obtain high-quality assembled genome sequences of these laboratory mouse strains, and what advances in sequencing technologies may be required to achieve this goal.
    Mammalian Genome 07/2012; 23(9-10):490-8. DOI:10.1007/s00335-012-9402-6 · 3.07 Impact Factor
Show more