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Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race

BACKGROUND: The genomes of pathogens are thought to have evolved under selective pressure provided by the host in a coevolutionary arms race (the 'Red Queen's Hypothesis'). Traditionally, adaptation by pathogens is thought to rely not on whole chromosome dynamics but on gain/loss of s...

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Autores principales: Nunes, Alexandra, Nogueira, Paulo J, Borrego, Maria J, Gomes, João P
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2760880/
https://www.ncbi.nlm.nih.gov/pubmed/18947394
http://dx.doi.org/10.1186/gb-2008-9-10-r153
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author Nunes, Alexandra
Nogueira, Paulo J
Borrego, Maria J
Gomes, João P
author_facet Nunes, Alexandra
Nogueira, Paulo J
Borrego, Maria J
Gomes, João P
author_sort Nunes, Alexandra
collection PubMed
description BACKGROUND: The genomes of pathogens are thought to have evolved under selective pressure provided by the host in a coevolutionary arms race (the 'Red Queen's Hypothesis'). Traditionally, adaptation by pathogens is thought to rely not on whole chromosome dynamics but on gain/loss of specific genes, yielding differential abilities to infect distinct tissues. Thus, it is not known whether distinct host organs differently shape the genome of the same pathogen. We tested this hypothesis using Chlamydia trachomatis as model species, looking at 15 serovars that infect different organs: eyes, genitalia and lymph nodes. RESULTS: We analyzed over 51,000 base pairs from all serovars using various phylogenetic approaches and a non-phylogenetic indel-based algorithm to study the evolution of individual and concatenated loci. This survey comprised about 33% of all single nucleotide polymorphisms in C. trachomatis chromosomes. We present a model in which genome evolution indeed correlates with the cell type (epithelial versus lymph cells) and organ (eyes versus genitalia) that a serovar infects, illustrating an adaptation to physiologically distinct niches, and discarding genetic drift as the dominant evolutionary driving force. We show that radiation of serovars occurred primarily by accumulation of single nucleotide polymorphisms in intergenomic regions, housekeeping genes, and genes encoding hypothetical and cell envelope proteins. Furthermore, serovar evolution also correlates with ecological success, as the two most successful serovars showed a parallel evolution. CONCLUSION: We identified a single nucleotide polymorphism-based tissue-specific arms race for strains in the same species, reflecting global chromosomal dynamics. Studying such tissue-specific arms race scenarios is crucial for understanding pathogen-host interactions during the course of infectious diseases, in order to dissect pathogen biology and develop preventive and therapeutic strategies.
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spelling pubmed-27608802009-10-13 Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race Nunes, Alexandra Nogueira, Paulo J Borrego, Maria J Gomes, João P Genome Biol Research BACKGROUND: The genomes of pathogens are thought to have evolved under selective pressure provided by the host in a coevolutionary arms race (the 'Red Queen's Hypothesis'). Traditionally, adaptation by pathogens is thought to rely not on whole chromosome dynamics but on gain/loss of specific genes, yielding differential abilities to infect distinct tissues. Thus, it is not known whether distinct host organs differently shape the genome of the same pathogen. We tested this hypothesis using Chlamydia trachomatis as model species, looking at 15 serovars that infect different organs: eyes, genitalia and lymph nodes. RESULTS: We analyzed over 51,000 base pairs from all serovars using various phylogenetic approaches and a non-phylogenetic indel-based algorithm to study the evolution of individual and concatenated loci. This survey comprised about 33% of all single nucleotide polymorphisms in C. trachomatis chromosomes. We present a model in which genome evolution indeed correlates with the cell type (epithelial versus lymph cells) and organ (eyes versus genitalia) that a serovar infects, illustrating an adaptation to physiologically distinct niches, and discarding genetic drift as the dominant evolutionary driving force. We show that radiation of serovars occurred primarily by accumulation of single nucleotide polymorphisms in intergenomic regions, housekeeping genes, and genes encoding hypothetical and cell envelope proteins. Furthermore, serovar evolution also correlates with ecological success, as the two most successful serovars showed a parallel evolution. CONCLUSION: We identified a single nucleotide polymorphism-based tissue-specific arms race for strains in the same species, reflecting global chromosomal dynamics. Studying such tissue-specific arms race scenarios is crucial for understanding pathogen-host interactions during the course of infectious diseases, in order to dissect pathogen biology and develop preventive and therapeutic strategies. BioMed Central 2008 2008-10-23 /pmc/articles/PMC2760880/ /pubmed/18947394 http://dx.doi.org/10.1186/gb-2008-9-10-r153 Text en Copyright © 2008 Nunes et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research
Nunes, Alexandra
Nogueira, Paulo J
Borrego, Maria J
Gomes, João P
Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title_full Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title_fullStr Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title_full_unstemmed Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title_short Chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
title_sort chlamydia trachomatis diversity viewed as a tissue-specific coevolutionary arms race
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2760880/
https://www.ncbi.nlm.nih.gov/pubmed/18947394
http://dx.doi.org/10.1186/gb-2008-9-10-r153
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