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Paleomicrobiology of Human Tuberculosis

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  • Author: Helen D. Donoghue1
  • Editors: Michel Drancourt2, Didier Raoult3
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Centre for Clinical Microbiology, Division of Infection and Immunity, University College London, United Kingdom; 2: Aix Marseille Université Faculté de Médecine, Marseille, France; 3: Aix Marseille Université Faculté de Médecine, Marseille, France
  • Source: microbiolspec July 2016 vol. 4 no. 4 doi:10.1128/microbiolspec.PoH-0003-2014
  • Received 09 December 2014 Accepted 12 January 2015 Published 08 July 2016
  • Helen Donoghue, h.donoghue@ucl.ac.uk
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  • Abstract:

    Tuberculosis is a significant global disease today, so understanding its origins and history is important. It is primarily a lung infection and is transmitted by infectious aerosols from person to person, so a high population density encourages its spread. The causative organism is , an obligate pathogen in the complex that also contains closely related species, such as , that primarily infect animals. Typical bone lesions occur in about 5% of untreated infections. These can be recognized in historical and archaeological material, along with nonspecific paleopathology such as new bone formation (periostitis), especially on ribs. Based on such lesions, tuberculosis has been found in ancient Egypt, pre-Columbian America, and Neolithic Europe. The detection of ancient DNA (aDNA) by using PCR led to the development of the new field of paleomicrobiology. As a result, a large number of tuberculosis cases were recognized in mummified tissue and bones with nonspecific or no lesions. In parallel with these developments, cell wall lipid biomarkers have detected tuberculosis suggested by paleopathology and confirmed aDNA findings. In well-preserved cases, molecular typing has identified lineages and genotypes. The current interest in targeted enrichment, shotgun sequencing, and metagenomic analysis reveals ancient mixed infections with different strains and other pathogens. Identification of lineages from samples of known age enables the date of the emergence of strains and lineages to be calculated directly rather than by making assumptions on the rate of evolutionary change.

  • Citation: Donoghue H. 2016. Paleomicrobiology of Human Tuberculosis. Microbiol Spectrum 4(4):PoH-0003-2014. doi:10.1128/microbiolspec.PoH-0003-2014.

Key Concept Ranking

Immune System Proteins
0.6842642
Human Infectious Diseases
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Bacterial Cell Wall
0.45689926
Cell-Mediated Immune Response
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/content/journal/microbiolspec/10.1128/microbiolspec.PoH-0003-2014
2016-07-08
2017-09-26

Abstract:

Tuberculosis is a significant global disease today, so understanding its origins and history is important. It is primarily a lung infection and is transmitted by infectious aerosols from person to person, so a high population density encourages its spread. The causative organism is , an obligate pathogen in the complex that also contains closely related species, such as , that primarily infect animals. Typical bone lesions occur in about 5% of untreated infections. These can be recognized in historical and archaeological material, along with nonspecific paleopathology such as new bone formation (periostitis), especially on ribs. Based on such lesions, tuberculosis has been found in ancient Egypt, pre-Columbian America, and Neolithic Europe. The detection of ancient DNA (aDNA) by using PCR led to the development of the new field of paleomicrobiology. As a result, a large number of tuberculosis cases were recognized in mummified tissue and bones with nonspecific or no lesions. In parallel with these developments, cell wall lipid biomarkers have detected tuberculosis suggested by paleopathology and confirmed aDNA findings. In well-preserved cases, molecular typing has identified lineages and genotypes. The current interest in targeted enrichment, shotgun sequencing, and metagenomic analysis reveals ancient mixed infections with different strains and other pathogens. Identification of lineages from samples of known age enables the date of the emergence of strains and lineages to be calculated directly rather than by making assumptions on the rate of evolutionary change.

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Image of FIGURE 1
FIGURE 1

Paleopathology diagnostic for skeletal tuberculosis: Pott’s disease, angular kyphosis in Th8–L2. Hungary: Zalavár-Vársziget-Kápolna, juvenile, grave No. 17/03. Paleopathology highly suggestive of tuberculosis: evidence of infection shown by fusion of vertebrae (Th6–8) with slight gibbus, cavities, and traces of cold abscess (chronic lytic lesion). Hungary: Zalavár-Vársziget-Kápolna, juvenile, grave No. 74/03. Paleopathology showing nonspecific changes consistent with a tuberculosis infection; disseminated, small, new bone formations can be observed on the costal groove and on the inner surface of the ribs. Romania: Peteni, grave No. 107. (Courtesy of Tamás Hadju, Department of Biological Anthropology, Eötvös Loránd University, Budapest, Hungary. Fig. 1A, B reprinted from [ 95 ] with permission of the publisher. Fig. 1C reprinted from [ 96 ] with permission of the publisher.)

Source: microbiolspec July 2016 vol. 4 no. 4 doi:10.1128/microbiolspec.PoH-0003-2014
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Image of FIGURE 2
FIGURE 2

Evolutionary relationship between selected mycobacteria and members of the complex (MTBC). The MTBC was thought to arise as a clonal expansion from a smooth tubercle bacillus (STB) progenitor population. The animal-adapted ecotypes branch from a presumed human-adapted lineage of that is currently restricted to West Africa. Human-adapted strains are grouped into seven main lineages, each of which is primarily associated with a distinct geographical distribution. The dates of branching events are only crude estimates. (Courtesy of James E. Galaghan, Department of Biomedical Engineering, Bioinformatics Program and National Emerging Infectious Diseases Laboratory, Boston University, Boston, Massachusetts, USA, and Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts, USA. Reprinted from [ 97 ] with permission of the publisher.)

Source: microbiolspec July 2016 vol. 4 no. 4 doi:10.1128/microbiolspec.PoH-0003-2014
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FIGURE 3

A possible timeline of evolutionary events and archaeological data; the location for archaeological evidence is indicated in each box. Boxes outlined in black indicate morphological evidence only, whereas boxes outlined in red denote both morphological and molecular evidence. (Courtesy of James E. Galaghan, Department of Biomedical Engineering, Bioinformatics Program and National Emerging Infectious Diseases Laboratory, Boston University, Boston, Massachusetts, USA, and Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts, USA. Reprinted from [ 97 ] with permission of the publisher.)

Source: microbiolspec July 2016 vol. 4 no. 4 doi:10.1128/microbiolspec.PoH-0003-2014
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FIGURE 4

Structures of selected lipid biomarkers. The main components of each mycolic acid class are shown; each class comprises a limited range of homologous components with different chain lengths. Mycolipenic and mycocerosic acids; for each component, the ions () monitored on negative ion-chemical ionization gas chromatography-mass spectrometry (NICI-GCMS) of pentafluorobenzyl esters of these acids are given. (Courtesy of David E. Minnikin, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, UK.)

Source: microbiolspec July 2016 vol. 4 no. 4 doi:10.1128/microbiolspec.PoH-0003-2014
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