A mutation burst during the acute phase of Helicobacter pylori infection in humans and rhesus macaques

Linz, Bodo; Windsor, Helen M.; McGraw, John J.; Hansen, Lori M.; Gajewski, Joseph J.; Tomsho, Lynn P.; Hake, Caylie M.; Solnick, Jay V.; Schuster, Stephan C.; Marshall, Barry J.

doi:10.1038/ncomms5165

Cited by 85 publications

(79 citation statements)

References 39 publications

(50 reference statements)

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“…This concept has received little attention for bacteria, although it may apply to Helicobacter pylori. For H. pylori, the average clock rate was 1000-fold slower for bacterial lineages that separated more than 50 000 years ago (2.6 Â 10 27 ) [12] than the short-term clock rate (3 Â 10 24 ) measured immediately after initiating an infection [14], and chronic infections over years were associated with intermediate rates (1.4 Â 10 25 ) [15]. Short-term rates would therefore be inappropriate for calculating the tMRCA of H. pylori.…”

Section: Introductionmentioning

confidence: 99%

How old are bacterial pathogens?

Achtman¹

2016

Proc. R. Soc. B.

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Only few molecular studies have addressed the age of bacterial pathogens that infected humans before the beginnings of medical bacteriology, but these have provided dramatic insights. The global genetic diversity of Helicobacter pylori , which infects human stomachs, parallels that of its human host. The time to the most recent common ancestor (tMRCA) of these bacteria approximates that of anatomically modern humans, i.e. at least 100 000 years, after calibrating the evolutionary divergence within H. pylori against major ancient human migrations. Similarly, genomic reconstructions of Mycobacterium tuberculosis , the cause of tuberculosis, from ancient skeletons in South America and mummies in Hungary support estimates of less than 6000 years for the tMRCA of M. tuberculosis . Finally, modern global patterns of genetic diversity and ancient DNA studies indicate that during the last 5000 years plague caused by Yersinia pestis has spread globally on multiple occasions from China and Central Asia. Such tMRCA estimates provide only lower bounds on the ages of bacterial pathogens, and additional studies are needed for realistic upper bounds on how long humans and animals have suffered from bacterial diseases.

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Section: Introductionmentioning

confidence: 99%

How old are bacterial pathogens?

Achtman¹

2016

Proc. R. Soc. B.

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“…Not including host genes can be misleading when studying the evolution of parasites, because host-to-parasite HGT is a frequent phenomenon. The third factor that makes the phylogenetic analysis of viruses a very delicate matter is their high evolutionary rate, with both high mutation and recombination frequencies [53][54][55][56][57]. Viral sequences tend to evolve rapidly and, when they have cellular homologues, they can be very divergent.…”

Section: Giant Viruses Horizontal Gene Transfer and Long Branch Attrmentioning

confidence: 99%

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?

Moreira¹,

López‐García²

2015

Phil. Trans. R. Soc. B

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The recent discovery of diverse very large viruses, such as the mimivirus, has fostered a profusion of hypotheses positing that these viruses define a new domain of life together with the three cellular ones (Archaea, Bacteria and Eucarya). It has also been speculated that they have played a key role in the origin of eukaryotes as donors of important genes or even as the structures at the origin of the nucleus. Thanks to the increasing availability of genome sequences for these giant viruses, those hypotheses are amenable to testing via comparative genomic and phylogenetic analyses. This task is made very difficult by the high evolutionary rate of viruses, which induces phylogenetic artefacts, such as long branch attraction, when inadequate methods are applied. It can be demonstrated that phylogenetic trees supporting viruses as a fourth domain of life are artefactual. In most cases, the presence of homologues of cellular genes in viruses is best explained by recurrent horizontal gene transfer from cellular hosts to their infecting viruses and not the opposite. Today, there is no solid evidence for the existence of a viral domain of life or for a significant implication of viruses in the origin of the cellular domains.

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“…The long, intimate association of H. pylori with humans suggests a history of bacterial adaptation. Considerable attention has focused on specific genes involved in modulating adaptive immunity of the host (for a review see Yamaoka 2010 andSalama et al 2013) and on genomic changes occurring during acute and chronic H. pylori infection (Kennemann et al 2011;Linz et al 2014) as well as during H. pylori transmission between human hosts (Linz et al 2013). However, bacterial genome adaptation has not been investigated at the global level.…”

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confidence: 99%

Worldwide Population Structure, Long-Term Demography, and Local Adaptation of Helicobacter pylori

et al. 2015

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Helicobacter pylori is an important human pathogen associated with serious gastric diseases. Owing to its medical importance and close relationship with its human host, understanding genomic patterns of global and local adaptation in H. pylori may be of particular significance for both clinical and evolutionary studies. Here we present the first such whole genome analysis of 60 globally distributed strains, from which we inferred worldwide population structure and demographic history and shed light on interesting global and local events of positive selection, with particular emphasis on the evolution of San-associated lineages. Our results indicate a more ancient origin for the association of humans and H. pylori than previously thought. We identify several important perspectives for future clinical research on candidate selected regions that include both previously characterized genes (e.g., transcription elongation factor NusA and tumor necrosis factor alpha-inducing protein Tipa) and hitherto unknown functional genes.KEYWORDS adaptation; neutral evolution; human pathogens H ELICOBACTER pylori is a Gram-negative bacterium that infects the mucosa of the human stomach. It was first described in the 1980s, when it was initially identified in association with chronic gastritis and later causally linked to serious gastric pathologies such as gastric cancer and ulcers (Marshall and Warren 1984;Suerbaum and Michetti 2002). It infects .80% of humans in developing countries and, although its prevalence is lower in developed countries, nearly 50% of the worldwide human population is infected (Ghose et al. 2005;Salih 2009;Salama et al. 2013).Due to its clinical and evolutionary importance, there has been considerable research on mechanisms of H. pylori transmission, as well as on the population genetics and phylogenetic relationships among global isolates. Thus far, population genetic analyses have mainly focused on seven housekeeping genes (usually referred to as multilocus sequence typing or MLST), with the primary conclusions being that H. pylori strains appear highly structured, and their phylogeographic patterns correlate consistently with that of their human hosts. Given that the H. pylori-humans association is at least 100,000 years old (Moodley et al. 2012), the current population structure of H. pylori may be regarded as mirroring past human expansions and migrations Linz et al. 2007;Breurec et al. 2011) and thus help us shed light on yet unknown dynamics of local demographic processes in human evolution. However, despite the knowledge gained thus far, the long-term global demographic history of H. pylori has never been directly inferred. The long, intimate association of H. pylori with humans suggests a history of bacterial adaptation. Considerable attention has focused on specific genes involved in modulating adaptive immunity of the host (for a review see Yamaoka 2010 andSalama et al. 2013) and on genomic changes occurring during acute and chronic H. pylori infection (Kennemann et al. 2011;Linz et a...

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A mutation burst during the acute phase of Helicobacter pylori infection in humans and rhesus macaques

Cited by 85 publications

References 39 publications

How old are bacterial pathogens?

How old are bacterial pathogens?

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?

Worldwide Population Structure, Long-Term Demography, and Local Adaptation of Helicobacter pylori

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