Convergent Molecular Evolution of Genomic Cores in Salmonella enterica and Escherichia coli

Chattopadhyay, Sujay; Paul, Sandip; Kisiela, Dagmara I.; Linardopoulou, Elena V.; Sokurenko, Evgeni V.

doi:10.1128/jb.00552-12

Cited by 36 publications

(36 citation statements)

References 52 publications

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“…However, they did not exclude the possible existence of rare mutations or short indels that do provide selective advantages. We therefore developed a second, novel Hidden Markov Model (DHMM) (SI Appendix, SI Materials and Methods) to identify regions of clustered SNPs/indels in the core genome, such as would be expected under Darwinian selection (42). Similar to other programs based on Hidden Markov Models, DHMM assigns clustered nucleotides to multiple "states," but the emission parameters in DHMM were designed to ensure that some of these states correspond to regions that are under diversifying selection.…”

Section: Resultsmentioning

confidence: 99%

Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever

Zhou

McCann

Weill

et al. 2014

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

120

127

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Multiple epidemic diseases have been designated as emerging or reemerging because the numbers of clinical cases have increased. Emerging diseases are often suspected to be driven by increased virulence or fitness, possibly associated with the gain of novel genes or mutations. However, the time period over which humans have been afflicted by such diseases is only known for very few bacterial pathogens, and the evidence for recently increased virulence or fitness is scanty. Has Darwinian (diversifying) selection at the genomic level recently driven microevolution within bacterial pathogens of humans? Salmonella enterica serovar Paratyphi A is a major cause of enteric fever, with a microbiological history dating to 1898. We identified seven modern lineages among 149 genomes on the basis of 4,584 SNPs in the core genome and estimated that Paratyphi A originated 450 y ago. During that time period, the effective population size has undergone expansion, reduction, and recent expansion. Mutations, some of which inactivate genes, have occurred continuously over the history of Paratyphi A, as has the gain or loss of accessory genes. We also identified 273 mutations that were under Darwinian selection. However, most genetic changes are transient, continuously being removed by purifying selection, and the genome of Paratyphi A has not changed dramatically over centuries. We conclude that Darwinian selection is not responsible for increased frequency of enteric fever and suggest that environmental changes may be more important for the frequency of disease. pathogen evolution | historical reconstruction | phylogeography

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Section: Resultsmentioning

confidence: 99%

Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever

Zhou

McCann

Weill

et al. 2014

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

120

127

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“…We identified ten site-specific hotspot mutations affecting only ST3 and ST36. The occurrence of shared hotspot mutations is a strong sign of convergent evolution (Chattopadhyay et al, 2012). Although the precise role of these genes remains unclear, four of these genes encode proteins (cytochrome c551 peroxidase, short-chain dehydrogenase, MerR family transcriptional regulator and glutathione S-transferase) predicted to mediate the detoxification of reactive oxygen species, which can accumulate as a by-product of aerobic respiration or host immune defense during phagocytosis (Cabiscol et al, 2000).…”

Section: Discussionmentioning

confidence: 99%

Genomic evidence of adaptive evolution in emergent Vibrio parahaemolyticus ecotypes

Turner

Berthiaume

Morales

et al. 2016

Elementa: Science of the Anthropocene

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The ubiquitous marine bacterium Vibrio parahaemolyticus is a leading cause of illness associated with seafood consumption. The emergence of two genetically distinct ecotypes (ST3 and ST36) has led to an alarming increase in the size and frequency of disease outbreaks. We conducted a genomic comparison of 30 V. parahaemolyticus genomes that represent a diverse collection of 15 genetically distinct ecotypes, including newly sequenced representatives of ST3 and ST36, isolated from both clinical and environmental sources. A multistep evolutionary analysis showed that genes associated with sensing and responding to environmental stimuli have evolved under positive selection, identifying examples of convergent evolution between ST3 and ST36. A comparison of predicted proteomes indicated that ST3 and ST36 ecotypes laterally acquired tens of novel genes associated with a variety of functions including dormancy, homeostasis and membrane transport. Genes identified in this study play an apparent role in environmental fitness and may confer cross protection against stressors encountered in the human host. Together, these results show the evolution of stress response is an important genetic mechanism correlated with the recent emergence of the ST3 and ST36 ecotypes.

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“…Since these two serovars do not share close common ancestry [23], the results suggest independent acquisition as genomic islands via horizontal gene transfer. This leads us to speculate on the possible role of gene transfer in adaptive convergent evolution of Paratyphi A and Typhi, in addition to recombination [23] and mutation [11] as demonstrated by previous studies. Group-specific analysis, a unique feature of PanCoreGen, thus indicates its possible important contribution in understanding common virulence factors linked to specific disease manifestations.…”

Section: Resultsmentioning

confidence: 86%

“…We considered Salmonella enterica ParatyphiB SPB7 as the first reference genome, due to presence of most annotated genes. We then calculated the pairwise distance of concatenated 7 housekeeping genes used for multi-locus sequence typing [11, 21] of SPB7 with other 16 strains, and incorporated other genomes based on their increasing phylogenetic distance from SPB7.…”

Section: Resultsmentioning

confidence: 99%

PanCoreGen — Profiling, detecting, annotating protein-coding genes in microbial genomes

et al. 2015

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A large amount of genomic data, especially from multiple isolates of a single species, has opened new vistas for microbial genomics analysis. Analyzing pan-genome (i.e. the sum of genetic repertoire) of microbial species is crucial in understanding the dynamics of molecular evolution, where virulence evolution is of major interest. Here we present PanCoreGen – a standalone application for pan- and core-genomic profiling of microbial protein-coding genes. PanCoreGen overcomes key limitations of the existing pan-genomic analysis tools, and develops an integrated annotation-structure for species-specific pan-genomic profile. It provides important new features for annotating draft genomes/contigs and detecting unidentified genes in annotated genomes. It also generates user-defined group-specific datasets within the pan-genome. Interestingly, analyzing an example-set of Salmonella genomes, we detect potential footprints of adaptive convergence of horizontally transferred genes in two human-restricted pathogenic serovars – Typhi and Paratyphi A. Overall, PanCoreGen represents a state-of-the-art tool for microbial phylogenomics and pathogenomics study.

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Convergent Molecular Evolution of Genomic Cores in Salmonella enterica and Escherichia coli

Cited by 36 publications

References 52 publications

Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever

Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever

Genomic evidence of adaptive evolution in emergent Vibrio parahaemolyticus ecotypes

PanCoreGen — Profiling, detecting, annotating protein-coding genes in microbial genomes

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