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From Evolutionary Advantage to Disease Agents: Forensic Reevaluation of Host-Microbe Interactions and Pathogenicity

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  • Authors: Jessica I. Rivera-Pérez1, Alfredo A. González2, Gary A. Toranzos3
  • Editors: Raúl J. Cano4, Gary A. Toranzos5
    Affiliations: 1: Environmental Microbiology Laboratory, Department of Biology, University of Puerto Rico, Rio Piedras Campus, San Juan, Puerto Rico 00931; 2: Environmental Microbiology Laboratory, Department of Biology, University of Puerto Rico, Rio Piedras Campus, San Juan, Puerto Rico 00931; 3: Environmental Microbiology Laboratory, Department of Biology, University of Puerto Rico, Rio Piedras Campus, San Juan, Puerto Rico 00931; 4: California Polytechnic State University, San Luis Obispo, CA; 5: University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico
  • Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
  • Received 27 October 2016 Accepted 29 November 2016 Published 03 February 2017
  • Jessica I. Rivera-Pérez, [email protected]
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  • Abstract:

    As the “human microbiome era” continues, there is an increasing awareness of our resident microbiota and its indispensable role in our fitness as holobionts. However, the host-microbe relationship is not so clearly defined for some human symbionts. Here we discuss examples of “accidental pathogens,” meaning previously nonpathogenic and/or environmental microbes thought to have inadvertently experienced an evolutionary shift toward pathogenicity. For instance, symbionts such as and JC polyomavirus have been shown to have accompanied humans since prehistoric times and are still abundant in extant populations as part of the microbiome. And yet, the relationship between a subgroup of these microbes and their human hosts seems to have changed with time, and they have recently gained notoriety as gastrointestinal and neuropathogens, respectively. On the other hand, environmental microbes such as spp. have recently experienced a shift in host range and are now a major problem in industrialized countries as a result of artificial ecosystems. Other variables involved in this accidental phenomenon could be the apparent change or reduction in the diversity of human-associated microbiota because of modern medicine and lifestyles. All of this could result in an increased prevalence of accidental pathogens in the form of emerging pathogens.

  • Citation: Rivera-Pérez J, González A, Toranzos G. 2017. From Evolutionary Advantage to Disease Agents: Forensic Reevaluation of Host-Microbe Interactions and Pathogenicity. Microbiol Spectrum 5(1):EMF-0009-2016. doi:10.1128/microbiolspec.EMF-0009-2016.


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As the “human microbiome era” continues, there is an increasing awareness of our resident microbiota and its indispensable role in our fitness as holobionts. However, the host-microbe relationship is not so clearly defined for some human symbionts. Here we discuss examples of “accidental pathogens,” meaning previously nonpathogenic and/or environmental microbes thought to have inadvertently experienced an evolutionary shift toward pathogenicity. For instance, symbionts such as and JC polyomavirus have been shown to have accompanied humans since prehistoric times and are still abundant in extant populations as part of the microbiome. And yet, the relationship between a subgroup of these microbes and their human hosts seems to have changed with time, and they have recently gained notoriety as gastrointestinal and neuropathogens, respectively. On the other hand, environmental microbes such as spp. have recently experienced a shift in host range and are now a major problem in industrialized countries as a result of artificial ecosystems. Other variables involved in this accidental phenomenon could be the apparent change or reduction in the diversity of human-associated microbiota because of modern medicine and lifestyles. All of this could result in an increased prevalence of accidental pathogens in the form of emerging pathogens.

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Endosymbiosis: Homage to Lynn Margulis. Artist: Shoshanah Dubiner. This painting illustrates a portion of the incredible microbial complexity that existed on this planet when animals evolved, and thus the microbial soup in which all organisms developed. Image courtesy of the artist. Image credits: Endosymbiosis: Homage to Lynn Margulis, Shoshanah Dubiner, 2012. http://www.cybermuse.com.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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in Ötzi, the 5,300-year-old iceman. Reads specific to were detected via metagenomic analysis of DNA extracted from different regions of the gastrointestinal tract of Ötzi the Tyrolean Iceman. The area where the muscle control sample was obtained is highlighted as a diamond (picture on the left), and the gastrointestinal sampling sites are marked in the radiographic image using the following legend: star, stomach content; circle, small intestine; square, upper large intestine; triangle, lower large intestine. The number of -specific reads per million metagenomic reads is indicated by the colored gradient bar on the right. Figure reproduced from reference ( 71 ), with permission. Reproduced from reference ( 66 ), with permission.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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Lower fecal microbiome diversity associated with individuals from industrialized cultures. Clemente et al. ( 72 ) compared the bacterial diversity in feces from cultures with hunter-gatherer lifestyles compared to progressively more industrialized cultures. Phylogenetic diversity in feces from Yanomami and Guahibo Amerindians, Malawians, and U.S. individuals. A higher bacterial diversity was detected in feces from the Yanomami, an isolated, rural indigenous culture inhabiting the Amazon. In comparison, a slightly decreased fecal diversity was found in Guahibo Amerindians. However, a major decrease was detected in the diversity of the fecal microbiota in U.S. subjects. A pronounced decrease was also detected in the functional profiles of fecal microbiomes from U.S. subjects compared to cultures with more traditional lifestyles (figure not shown). Key differential bacterial groups between fecal microbiomes from Yanomami and Guahibo Amerindians, Malawians, and U.S. subjects. Functional diversity in feces from Yanomami and Guahibo Amerindians, Malawians, and U.S. individuals. As expected, a higher overall functional diversity was detected in Yanomami Amerindians. Comparison of major metabolic pathways detected in fecal microbiomes from Yanomami and Guahibo Amerindians, Malawians, and U.S. subjects. Reproduced from reference ( 72 ), with permission.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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Forensic studies with JCV DNA suggest that the expansion of from prehistoric Africa occurred as a two-migration model. As Pavesi shows in his model, two out-of-Africa migrations were suggested by currently characterized JCV subtypes. The first migration, represented with a solid line, is compatible with that previously suggested by human genes. The second migration, traced with a dashed line, indicates an additional route of expansion suggested by JCV but that is undetectable using only human genes. Reproduced from reference ( 209 ), with permission.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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Origin of human-associated . Although its exact ancestral history remains unresolved, recent studies clearly suggest that was associated with humans previous to their expansion from prehistoric Africa. However, is believed to have been an environmental microbe long before its association with ancient humans. This figure was taken from reference ( 210 ), with permission, and depicts a summary of the conclusions implied by current phylogenetic literature on the evolution of and other members of the complex.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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infections in environmental amoebae and human macrophages. Electron micrographs of U937 macrophages and infected by (strain AA100) at 24 h. Reproduced from reference ( 211 ), with permission.

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016
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Definition of terms used throughout this review

Source: microbiolspec February 2017 vol. 5 no. 1 doi:10.1128/microbiolspec.EMF-0009-2016

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