Natural Selection Promotes Antigenic Evolvability

Graves, C. J.; Ros, V.I.D.; Stevenson, Brian; Sniegowski, Paul D.; Brisson, Dustin

doi:10.1371/journal.ppat.1003766

Cited by 46 publications

(61 citation statements)

References 60 publications

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“…However, a recent study (75) showed that immune sera from Peromyscus leucopus infected with various B. burgdorferi strains contained no cross-reactive antiVlsE antibodies compared to the more broadly cross-reactive immunoglobulins observed in laboratory mice and other animals (71,76,77), suggesting that the repertoire of anti-VlsE antibodies is more limited during infection of the natural reservoir host. Additionally, repertoire differences can result from diversity among the vls silent cassette sequences of heterologous B. burgdorferi strains due to the recently reported evolvability of the B. burgdorferi vls system (78). Experiments utilizing Peromyscus mice challenged by tick-derived secondary B. burgdorferi clones are ongoing to address whether the limited anti-VlsE repertoire affects the outcome of host superinfection.…”

Section: Discussionmentioning

confidence: 99%

Bacterial Heterogeneity Is a Requirement for Host Superinfection by the Lyme Disease Spirochete

Rogovskyy

Bankhead

2014

Infect Immun

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In nature, mixed Borrelia burgdorferi infections are common and possibly can be acquired by either superinfection or coinfection. Superinfection by heterologous B. burgdorferi strains has been established experimentally, although the ability of homologous B. burgdorferi clones to superinfect a host has not been studied in detail. Information regarding any potential immune barriers to secondary infection also currently is unavailable. In the present study, the ability to superinfect various mouse models by homologous wild-type clones was examined and compared to superinfection by heterologous strains. To assess the ability of homologous B. burgdorferi clones to successfully superinfect a mouse host, primary-and secondary-infecting spirochetes were recovered via in vitro cultivation of collected blood or tissue samples. This was accomplished by generating two different antibiotic-resistant versions of the wild-type B31-A3 clone in order to distinguish superinfecting B. burgdorferi from primary-infecting spirochetes. The data demonstrate an inability of homologous B. burgdorferi to superinfect immunocompetent mice as opposed to heterologous strains. Attempts to superinfect different types of immunodeficient mice with homologous B. burgdorferi indicate that the murine innate immune system represents a major barrier to intrastrain superinfection. Consequently, the possibility of innate immunity as a driving force for B. burgdorferi heterogeneity during the enzootic cycle is discussed.

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Section: Discussionmentioning

confidence: 99%

Bacterial Heterogeneity Is a Requirement for Host Superinfection by the Lyme Disease Spirochete

Rogovskyy

Bankhead

2014

Infect Immun

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“…One of many documented examples is the ability of bacterium Borrelia burgdorferi to evolve additional evolvability towards acquiring alterations of key antigen epitopes recognized by its host's immune system-alterations that confer clear survival advantage to the organism by enabling it to escape immune responses (Graves et al 2013). The effect of coevolution on evolvability has also been explored and confirmed by mathematical modelling ("evolutionary experiment") performed by Zaman et al (2014).…”

Section: Understanding Evolvabilitymentioning

confidence: 99%

Evolvability Is an Evolved Ability: The Coding Concept as the Arch-Unit of Natural Selection

Janković

Ćirković

2015

Orig Life Evol Biosph

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Physical processes that characterize living matter are qualitatively distinct in that they involve encoding and transfer of specific types of information. Such information plays an active part in the control of events that are ultimately linked to the capacity of the system to persist and multiply. This algorithmicity of life is a key prerequisite for its Darwinian evolution, driven by natural selection acting upon stochastically arising variations of the encoded information. The concept of evolvability attempts to define the total capacity of a system to evolve new encoded traits under appropriate conditions, i.e., the accessible section of total morphological space. Since this is dependent on previously evolved regulatory networks that govern information flow in the system, evolvability itself may be regarded as an evolved ability. The way information is physically written, read and modified in living cells (the "coding concept") has not changed substantially during the whole history of the Earth's biosphere. This biosphere, be it alone or one of many, is, accordingly, itself a product of natural selection, since the overall evolvability conferred by its coding concept (nucleic acids as information carriers with the "rulebook of meanings" provided by codons, as well as all the subsystems that regulate various conditional information-reading modes) certainly played a key role in enabling this biosphere to survive up to the present, through alterations of planetary conditions, including at least five catastrophic events linked to major mass extinctions. We submit that, whatever the actual prebiotic physical and chemical processes may have been on our home planet, or may, in principle, occur at some time and place in the Universe, a particular coding concept, with its respective potential to give rise to a biosphere, or class of biospheres, of a certain evolvability, may itself be regarded as a unit (indeed the arch-unit) of natural selection.

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“…The difference between any two VlsE variants within a host is a function of the number of recombination events that have occurred since the variants shared a common ancestor and the number of amino acids altered per recombination event. The number of amino acids altered per recombination event depends upon the sequence diversity among the vls cassettes that recombine into vlsE [24]. The distributions of sequence similarities between pairs of VlsE variants were estimated by explicitly simulating recombination between unexpressed vls cassettes and the expression site.…”

Section: Antigenic Variationmentioning

confidence: 99%

“…Novel VlsE variants are generated by unidirectional recombination of a random segment from one of several unexpressed, paralogous vls cassettes into the vlsE expression site [19,20], creating subpopulations of B. burgdorferi with novel VlsE sequences [21]. The magnitude of diversity among VlsE variants generated by the vls antigenic variation system is correlated with the ability to evade antibody recognition and permit chronic infections [16][17][18][19][22][23][24][25][26].…”

Section: Introductionmentioning

confidence: 99%

Interactions between host immune response and antigenic variation that control Borrelia burgdorferi population dynamics

Zhou

Brisson

2017

Microbiology

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The population dynamics of pathogens within hosts result from interactions between host immune responses and mechanisms of the pathogen to evade or resist immune responses. Vertebrate hosts have evolved adaptive immune responses to eliminate the infection, while many pathogens evade immune clearance through altering surface antigens. Such interactions can result in a characteristic pattern of pathogen population dynamics within hosts consisting of population growth after infection, rapid population decline following specific immune responses, followed by persistence at low densities during a chronic infection stage. Despite the medical importance of chronic infections, little is known about the conditions of the interactions between variable antigens and the adaptive immune system that cause the characteristic pathogen population dynamics. Using the vls antigenic variation system of the Lyme disease pathogen, Borrelia burgdorferi, as a model system, we investigated conditions of the interaction between the antigenic variation system and the adaptive immune response that can explain the within-host population dynamics of B. burgdorferi using mathematical modelling. This characteristic population dynamic pattern can be explained by models that assume a variable immune removal rate of antibody-bound B. burgdorferi. However, models with a constant immune removal rate could reproduce the rapid population decline of B. burgdorferi populations but not their longterm persistence within hosts using parameter values determined by fitting empirical data. The model predictions, along with the assumptions about the interactions between B. burgdorferi and the immune response, can be tested experimentally to estimate the likelihood that each mechanism affects B. burgdorferi population dynamics in real infections.

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Natural Selection Promotes Antigenic Evolvability

Cited by 46 publications

References 60 publications

Bacterial Heterogeneity Is a Requirement for Host Superinfection by the Lyme Disease Spirochete

Bacterial Heterogeneity Is a Requirement for Host Superinfection by the Lyme Disease Spirochete

Evolvability Is an Evolved Ability: The Coding Concept as the Arch-Unit of Natural Selection

Interactions between host immune response and antigenic variation that control Borrelia burgdorferi population dynamics

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