Overview and phylogeny of Mycobacterium tuberculosis complex organisms: Implications for diagnostics and legislation of bovine tuberculosis

doi:10.1016/j.rvsc.2014.02.009

Research in Veterinary Science

Volume 97, Supplement, October 2014, Pages S5-S19

https://doi.org/10.1016/j.rvsc.2014.02.009 Get rights and content

Abstract

Members of the Mycobacterium tuberculosis complex (MTBC) cause a serious disease with similar pathology, tuberculosis; in this review, bovine tuberculosis will be considered as disease caused by any member of the MTBC in bovids. Bovine tuberculosis is responsible for significant economic loss due to costly eradication programs and trade limitations and poses a threat to both endangered and protected species as well as to public health. We here give an overview on all members of the MTBC, focusing on their isolation from different animal hosts. We also review the recent advances made in elucidating the evolutionary and phylogenetic relationships of members of the MTBC. Because the nomenclature of the MTBC is controversial, its members have been considered species, subspecies or ecotypes, this review discusses the possible implications for diagnostics and the legal consequences of naming of new species.

Introduction

Mycobacterial species causing tuberculosis in humans and animals are merged in the Mycobacterium tuberculosis complex (MTBC). To date, the following organisms are considered members of the MTBC: M. tuberculosis (Koch, 1882), Mycobacterium bovis (Karlson and Lessel, 1970), M. bovis Bacillus Calmette and Guérin (BCG) (Guérin and Rosenthal, 1957), Mycobacterium africanum (Castets et al., 1968, Castets and Sarrat, 1969), Mycobacterium microti (Wells and Oxon, 1937, Reed, 1957), Mycobacterium canettii (van Soolingen et al., 1997), Mycobacterium pinnipedii (Cousins et al., 2003), and Mycobacterium caprae (Aranaz et al., 2003); moreover, the MTBC includes the oryx bacillus (Lomme et al., 1976) that has recently been proposed to be elevated to Mycobacterium orygis (van Ingen et al., 2012) and the dassie bacillus (Wagner et al., 1958). A pathogen of mongooses similar to the dassie bacillus has been suggested to be named Mycobacterium mungi (Alexander et al., 2010).

The division into different species is based on host preference, supported by molecular phylogenetics (Brosch et al., 2002). However, it has been suggested that the MTBC may instead represent a series of host-adapted clades consistent with the ecotype concept of Cohan (Cohan, 2002, Smith et al., 2006a). Nevertheless, these species, or ecotypes, can be distinguished by their distinct cultural and biochemical characteristics (Collins and de Lisle, 1985, Grange et al., 1996).

We review the members of the MTBC and their range of hosts, the phylogenetic markers that have been used to-date in order to identify lineages or clonal complexes relevant for tuberculosis in animals and describe the phylogeny and spread of these pathogens. Finally, we discuss the implications that naming new species within the MTBC may have on legislation of animal tuberculosis.

Section snippets

The M. tuberculosis complex

The MTBC is characterised by 99.9% similarity at the nucleotide level and virtually identical 16S rRNA sequences (Böddinghaus et al., 1990, Sreevatsan et al., 1997, Huard et al., 2006). Strains of the MTBC have a highly clonal population structure with little or no evidence for recombination (exchange of chromosomal DNA) between strains (Supply et al., 2003, Smith et al., 2006b, Hershberg et al., 2008). An analysis of 24 whole genome sequences of M. tuberculosis using four different methods

Phylogenetic markers

A variety of DNA fingerprinting methods have been used for epidemiological purposes and phylogenetic studies in M. tuberculosis, for detailed description of the techniques see recent reviews (Schürch and van Soolingen, 2012, Gormley et al., this issue). The suitability of a deletion as a phylogenetic marker depends on the stability and essentiality of the affected genomic region; deletions in regions with a high mutation rate, such as regions with nonessential genes or with repetitive DNA may

Phylogeny of the M. tuberculosis complex

The most universally accepted description of the phylogeny of all members of the MTBC is based on the analysis of RDs and a selection of SNPs (Brosch et al., 2002). This phylogeny suggests that an organism with the essential properties of M. tuberculosis is the ancestor of all members of the MTBC (Smith et al., 2009b, Fig. 1). These studies concluded that the strains host-adapted to animals formed a nested lineage marked by the absence of the specific RD9 (Brosch et al., 2002, Smith et al.,

Population genetics and spread of M. bovis and M. caprae

Modern genetic and archaeological evidence suggests that the domestication of European cattle took place in the Near East at the beginning of the Neolithic (Beja-Pereira et al., 2006, Edwards et al., 2007). Those studies are based on mitochondrial DNA of cattle origin and allow a hypothesis on the expansion of cattle from an ancestral population in the Fertile Crescent (including today’s Iraq, Syria, Jordan, Israel, Lebanon, the West Bank and parts of Egypt, Iran and Turkey) (Götherström et

Implications for diagnostics

Regarding the pathological findings, there are only a small number of studies dealing with potential differences in pathology among MTBC species or strains. Strain diversity in M. tuberculosis might be related to differences in severity of disease and transmissibility (Caws et al., 2008). It is currently unknown whether the reason underlying the preference for a certain animal host species has a genetic basis or depends only of the epidemiological situation. In animals, both M. bovis and M.

Legal implications

M. bovis is considered the main causative agent of animal tuberculosis and the term “bovine tuberculosis” has often been confusingly used to refer to infection by M. bovis in any species. Yet, according to the Task Force Bovine Tuberculosis Subgroup (2006) bovine tuberculosis is the “Infection in cattle with any of the disease-causing mycobacterial species within the M. tuberculosis complex”. Bovine tuberculosis is a listed disease of the OIE (World Organisation for Animal Health) and M. caprae

Conclusion

Formal designation of the members of the MTBC is controversial as they have been considered species, subspecies or host-adapted ecotypes depending on the strict taxonomical criteria used for interpretation. For convenience and tradition the concept of “species” based on host-preference and some constant characteristics seems to prevail mainly to reflect a potential source for the infection in the epidemiological studies. However, as the sequence diversity within the whole of the MTBC is less

Acknowledgements

We would like to thank the National Authorities and Reference Laboratories for providing information on legislation regarding animal tuberculosis and Prof. Mark Chambers for careful revision and comments on the manuscript. We would like to acknowledge all partners funded by European Projects SSPE-CT-2004-501903 (VENoMYC) and FP7-KBBE-2007-1 (TB-Step). SRC is grateful for the support received from the Swiss Federal Veterinary Office and would like to acknowledge her former colleagues from the

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Overview and phylogeny of Mycobacterium tuberculosis complex organisms: Implications for diagnostics and legislation of bovine tuberculosis

Abstract

Introduction

Section snippets

The M. tuberculosis complex

Phylogenetic markers

Phylogeny of the M. tuberculosis complex

Population genetics and spread of M. bovis and M. caprae

Implications for diagnostics

Legal implications

Conclusion

Acknowledgements

Infection Genetics and Evolution

Pathologie Biologie (Paris)

Infection Genetics and Evolution

The Veterinary Journal

The Veterinary Journal

The Veterinary Journal

Vaccine

FEMS Microbiology Letters

Diagnostic Microbiology and Infectious Disease

Small Ruminant Research

The Veterinary Journal

Tubercle

Tuberculosis (Edinburgh)

Veterinary Microbiology

Veterinary Microbiology

Veterinary Microbiology

Lancet

The Lancet Infectious Diseases

Research in Veterinary Science

Mycobacterium tuberculosis: an emerging disease of free-ranging wildlife

Emerging Infectious Diseases

Novel Mycobacterium tuberculosis complex pathogen, M. mungi

Emerging Infectious Diseases

Importance of identifying Mycobacterium bovis as a causative agent of human tuberculosis

European Respiratory Journal

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High prevalence and increased severity of pathology of bovine tuberculosis in Holsteins compared to zebu breeds under field cattle husbandry in central Ethiopia

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Journal of Clinical Microbiology

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Veterinary Record

Mycobacterium tuberculosis subsp. caprae subsp. nov.: a taxonomic study of a new member of the Mycobacterium tuberculosis complex isolated from goats in Spain

International Journal of Systematic Bacteriology

Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. (1999) to species rank as Mycobacterium caprae comb. nov., sp. nov

International Journal of Systematic and Evolutionary Microbiology

Spoligotyping profile change caused by deletion of a direct variable repeat in a Mycobacterium tuberculosis isogenic laboratory strain

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Veterinary Record

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Veterinary Record

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Journal of Wildlife Diseases

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The origin of European cattle: evidence from modern and ancient DNA

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An outbreak of bovine tuberculosis in a free-living African buffalo (Syncerus caffer-sparrman) population in the Krüger National Park: a preliminary report

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African 2, a Clonal Complex of Mycobacterium bovis Epidemiologically Important in East Africa

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Tuberculosis in sea lions and fur seals from the south-western Atlantic coast

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Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations

PLoS Pathogens

Detection and identification of mycobacteria by amplification of rRNA

Journal of Clinical Microbiology

Molecular typing of Mycobacterium bovis strains isolated in Italy from 2000 to 2006 and evaluation of variable-number-tandem-repeats for a geographic optimized genotyping

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Tuberculose chez un chamois