Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes

Lieberman, Tami D.; Michel, Jean-Baptiste; Aingaran, Mythili; Potter-Bynoe, Gail; Roux, Damien; Davis, Michael R.; Skurnik, David; Leiby, Nicholas; LiPuma, John J.; Goldberg, Joanna B.; McAdam, Alexander J.; Priebe, Gregory P.; Kishony, Roy

doi:10.1038/ng.997

Cited by 361 publications

(489 citation statements)

References 38 publications

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“…We next determined the degree of genetic variation at each of the 1,931 loci present in the core genome for the 194 ST-1 strains to ask the question whether particular GBS genes have high levels of genetic variation, as such loci would be expected to participate in host-pathogen interaction (32). After accounting for multiple comparisons, 31 genes had significantly higher genetic variation levels compared with the remainder of the genome (Fig.…”

Section: High Rates Of Antimicrobial Resistance Genes Present In St-1mentioning

confidence: 99%

Sequence type 1 group B Streptococcus , an emerging cause of invasive disease in adults, evolves by small genetic changes

Galloway-Peña

Sahasrabhojane

Saldaña

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

101

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The molecular mechanisms underlying pathogen emergence in humans is a critical but poorly understood area of microbiologic investigation. Serotype V group B Streptococcus (GBS) was first isolated from humans in 1975, and rates of invasive serotype V GBS disease significantly increased starting in the early 1990s. We found that 210 of 229 serotype V GBS strains (92%) isolated from the bloodstream of nonpregnant adults in the United States and Canada between 1992 and 2013 were multilocus sequence type (ST) 1. Elucidation of the complete genome of a 1992 ST-1 strain revealed that this strain had the highest homology with a GBS strain causing cow mastitis and that the 1992 ST-1 strain differed from serotype V strains isolated in the late 1970s by acquisition of cell surface proteins and antimicrobial resistance determinants. Whole-genome comparison of 202 invasive ST-1 strains detected significant recombination in only eight strains. The remaining 194 strains differed by an average of 97 SNPs. Phylogenetic analysis revealed a temporally dependent mode of genetic diversification consistent with the emergence in the 1990s of ST-1 GBS as major agents of human disease. Thirty-one loci were identified as being under positive selective pressure, and mutations at loci encoding polysaccharide capsule production proteins, regulators of pilus expression, and two-component gene regulatory systems were shown to affect the bacterial phenotype. These data reveal that phenotypic diversity among ST-1 GBS is mainly driven by small genetic changes rather than extensive recombination, thereby extending knowledge into how pathogens adapt to humans.Streptococcus agalactiae | pathogenesis | evolution | single nucleotide polymorphisms | surface protein

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Section: High Rates Of Antimicrobial Resistance Genes Present In St-1mentioning

confidence: 99%

Sequence type 1 group B Streptococcus , an emerging cause of invasive disease in adults, evolves by small genetic changes

Galloway-Peña

Sahasrabhojane

Saldaña

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

101

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“…Recently, time-resolved sequencing of microbial evolution experiments 1–6 , viral and bacterial infections 7–9 , and cancers 10 has begun to illuminate this process. These studies reveal complex dynamics, characterized by rapid adaptation, competition between beneficial mutations, diminishing-returns epistasis, and extensive genetic parallelism.…”

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confidence: 99%

The dynamics of molecular evolution over 60,000 generations

Good

McDonald

Barrick

et al. 2017

Nature

670

839

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The outcomes of evolution are determined by a stochastic dynamical process that governs how mutations arise and spread through a population. Here, we analyze the dynamics of molecular evolution in twelve experimental populations of Escherichia coli, using whole-genome metagenomic sequencing at 500-generation intervals through 60,000 generations. Despite a declining rate of fitness gain, molecular evolution continues to be characterized by signatures of rapid adaptation, with multiple beneficial variants simultaneously competing for dominance in each population. Interactions between ecological and evolutionary processes play an important role, as long-term quasi-stable coexistence arises spontaneously in most populations, and evolution continues within each clade. We also present new evidence that the targets of natural selection change over time, as epistasis and historical contingency alter the strength of selection on different genes. Together, these results show that long-term adaptation to a constant environment can be a more complex and dynamic process than is often assumed.

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“…These changes are often polarized into two classes: those that affect protein structure and those that affect protein expression level. Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3,4), and their relative importance has been the topic of considerable discussion (5)(6)(7)(8)(9)(10)(11)(12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13)(14)(15)(16) or selective regimes (17)(18)(19)(20)(21)(22).…”

mentioning

confidence: 99%

The predictability of molecular evolution during functional innovation

Blank

Wolf

Ackermann

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Determining the molecular changes that give rise to functional innovations is a major unresolved problem in biology. The paucity of examples has served as a significant hindrance in furthering our understanding of this process. Here we used experimental evolution with the bacterium Escherichia coli to quantify the molecular changes underlying functional innovation in 68 independent instances ranging over 22 different metabolic functions. Using whole-genome sequencing, we show that the relative contribution of regulatory and structural mutations depends on the cellular context of the metabolic function. In addition, we find that regulatory mutations affect genes that act in pathways relevant to the novel function, whereas structural mutations affect genes that act in unrelated pathways. Finally, we use population genetic modeling to show that the relative contributions of regulatory and structural mutations during functional innovation may be affected by population size. These results provide a predictive framework for the molecular basis of evolutionary innovation, which is essential for anticipating future evolutionary trajectories in the face of rapid environmental change.adaptation | transcription | compensatory mutation | biosynthesis O ne of the most important questions in evolutionary biology concerns the molecular mechanisms that underlie functional innovations. These changes are often polarized into two classes: those that affect protein structure and those that affect protein expression level. Both of these classes have been shown to play important roles across a wide range of taxa, from vertebrates (1, 2) to bacteria (3, 4), and their relative importance has been the topic of considerable discussion (5-12). Significantly, many previous studies have addressed these questions by focusing on single instances of functional innovation (13-16) or selective regimes (17)(18)(19)(20)(21)(22). However, to identify general principles, it is necessary to study evolutionary innovation for a large number of different functions in parallel. Indeed, the fact that only a small number of examples exist has resulted in few hypotheses being put forth that identify general characteristics of the molecular changes underlying functional innovation. One prominent hypothesis states that if the development of a novel trait is spatially or temporally limited, then innovation frequently occurs through changes in regulation (23,24). Whether there are general patterns beyond this is not well-established.Here we used an experimental system that allows the analysis of a large number of independent cases of evolutionary innovation and investigation of the underlying genetic changes. We worked with a collection of 87 strains of Escherichia coli that each had a deletion of one gene encoding a different metabolic function (SI Appendix, Table S1). Each of these deletions resulted in an inability to grow in minimal glucose media. Then, for each of these 87 deleted metabolic functions, we used experimental evolution to select for novel func...

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Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes

Cited by 361 publications

References 38 publications

Sequence type 1 group B Streptococcus , an emerging cause of invasive disease in adults, evolves by small genetic changes

Sequence type 1 group B Streptococcus , an emerging cause of invasive disease in adults, evolves by small genetic changes

The dynamics of molecular evolution over 60,000 generations

The predictability of molecular evolution during functional innovation

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