Published December 1, 2021
| Version 2
Journal article
Open
A new nomenclature for the livestock-associated Mycobacterium tuberculosiscomplex based on phylogenomics
Creators
- 1. University of Basel, Basel, Switzerland
- 2. Department of Medical Microbiology, Ege University Faculty of Medicine, Izmir, Turkey
- 3. Institute for Food Safety and Hygiene, Section of Veterinary Bacteriology, University of Zurich, Zurich, Switzerland
- 4. National Reference Centre for Bovine Tuberculosis, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia Romagna, Brescia, Italy
- 5. Risk Analysis and Genomic Epidemiology Unit, Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna, Parma, Italy
- 6. Department of Medical Microbiology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
Description
Background
The bacteria that compose the Mycobacterium tuberculosis complex (MTBC) cause tuberculosis (TB) in humans and in different animals, including livestock. Much progress has been made in understanding the population structure of the human-adapted members of the MTBC by combining phylogenetics with genomics. Accompanying the discovery of new genetic diversity, a body of operational nomenclature has evolved to assist comparative and molecular epidemiological studies of human TB. By contrast, for the livestock-associated MTBC members, Mycobacterium bovis, M. caprae and M. orygis, there has been a lack of comprehensive nomenclature to accommodate new genetic diversity uncovered by emerging phylogenomic studies. We propose to fill this gap by putting forward a new nomenclature covering the main phylogenetic groups within M. bovis, M. caprae and M. orygis.
Methods
We gathered a total of 8,736 whole-genome sequences (WGS) from public sources and 39 newly sequenced strains, and selected a subset of 829 WGS, representative of the worldwide diversity of M. bovis, M. caprae and M. orygis. We used phylogenetics and genetic diversity patterns inferred from WGS to define groups.
Results
We propose to divide M. bovis, M. caprae and M. orygis in three main phylogenetic lineages, which we named La1, La2 and La3, respectively. Within La1, we identified several monophyletic groups, which we propose to classify into eight sublineages (La1.1-La1.8). These sublineages differed in geographic distribution, with some being geographically restricted and others globally widespread, suggesting different expansion abilities. To ease molecular characterization of these MTBC groups by the community, we provide phylogenetically informed, single nucleotide polymorphisms that can be used as barcodes for genotyping. These markers were implemented in KvarQ and TB-Profiler, which are platform-independent, open-source tools.
Conclusions
Our results contribute to an improved classification of the genetic diversity within the livestock-associated MTBC, which will benefit future molecular epidemiological and evolutionary studies.
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References
- (2020). Global Tuberculosis Report.
- Ayele WY, Neill SD, Zinsstag J (2004). Bovine tuberculosis: an old disease but a new threat to Africa. Int J Tuberc Lung Dis.
- Reviriego Gordejo FJ, Vermeersch JP (2006). Towards eradication of bovine tuberculosis in the European Union. Vet Microbiol. doi:10.1016/j.vetmic.2005.11.034
- Brites D, Loiseau C, Menardo F (2018). A New Phylogenetic Framework for the Animal-Adapted Complex. Front Microbiol. doi:10.3389/fmicb.2018.02820
- Bolotin E, Hershberg R (2015). Gene Loss Dominates As a Source of Genetic Variation within Clonal Pathogenic Bacterial Species. Genome Biol Evol. doi:10.1093/gbe/evv135
- Godfroid M, Dagan T, Kupczok A (2018). Recombination Signal in Stems from Reference-guided Assemblies and Alignment Artefacts. Genome Biol Evol. doi:10.1093/gbe/evy143
- Namouchi A, Didelot X, Schöck U (2012). After the bottleneck: Genome-wide diversification of the complex by mutation, recombination, and natural selection. Genome Res. doi:10.1101/gr.129544.111
- Boritsch EC, Khanna V, Pawlik A (2016). Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria. Proc Natl Acad Sci U S A. doi:10.1073/pnas.1604921113
- Malone KM, Gordon SV (2017). Complex Members Adapted to Wild and Domestic Animals. Adv Exp Med Biol. doi:10.1007/978-3-319-64371-7_7
- Ngabonziza JCS, Loiseau C, Marceau M (2020). A sister lineage of the complex discovered in the African Great Lakes region. Nat Commun. doi:10.1038/s41467-020-16626-6
- Coscolla M, Gagneux S, Menardo F (2021). Phylogenomics of reveals a new lineage and a complex evolutionary history. Microb Genom. doi:10.1099/mgen.0.000477
- Villarreal-Ramos B, Berg S, Whelan A (2018). Experimental infection of cattle with Mycobacterium tuberculosis isolates shows the attenuation of the human tubercle bacillus for cattle. Sci Rep. doi:10.1038/s41598-017-18575-5
- Smith NH, Berg S, Dale J (2011). European 1: a globally important clonal complex of. Infect Genet Evol. doi:10.1016/j.meegid.2011.04.027
- Rodriguez-Campos S, Schürch AC, Dale J (2012). European 2--a clonal complex of dominant in the Iberian Peninsula. Infect Genet Evol. doi:10.1016/j.meegid.2011.09.004
- Berg S, Garcia-Pelayo MC, Müller B (2011). African 2, a clonal complex of epidemiologically important in East Africa. J Bacteriol. doi:10.1128/JB.00750-10
- Müller B, Hilty M, Berg S (2009). African 1, An Epidemiologically Important Clonal Complex of Dominant in Mali, Nigeria, Cameroon, and Chad. J Bacteriol. doi:10.1128/JB.01590-08
- Loiseau C, Menardo F, Aseffa A (2020). An African origin for. Evol Med Public Health. doi:10.1093/emph/eoaa005
- da Conceição ML, Conceição EC, Furlaneto IP (2020). Phylogenomic Perspective on a Unique Clade Dominating Bovine Tuberculosis Infections among Cattle and Buffalos in Northern Brazil. Sci Rep. doi:10.1038/s41598-020-58398-5
- Zimpel CK, Patané JSL, Guedes ACP (2020). Global Distribution and Evolution of Lineages. Front Microbiol. doi:10.3389/fmicb.2020.00843
- Kohl TA, Kranzer K, Andres S (2020). Population Structure of in Germany: a Long-Term Study Using Whole-Genome Sequencing Combined with Conventional Molecular Typing Methods. J Clin Microbiol. doi:10.1128/JCM.01573-20
- Hauer A, Michelet L, Cochard T (2019). Accurate Phylogenetic Relationships Among Strains Circulating in France Based on Whole Genome Sequencing and Single Nucleotide Polymorphism Analysis. Front Microbiol. doi:10.3389/fmicb.2019.00955
- van Ingen J, Rahim Z, Mulder A (2012). Characterization of complex subspecies. Emerg Infect Dis. doi:10.3201/eid1804.110888
- Rahim Z, Thapa J, Fukushima Y (2017). Tuberculosis Caused by in Dairy Cattle and Captured Monkeys in Bangladesh: a New Scenario of Tuberculosis in South Asia. Transbound Emerg Dis. doi:10.1111/tbed.12596
- Thapa J, Nakajima C, Maharjan B (2015). Molecular characterization of isolates from wild animals of Nepal. Jpn J Vet Res. doi:10.14943/jjvr.63.3.151
- Duffy SC, Srinivasan S, Schilling MA (2020). Reconsidering as a proxy for zoonotic tuberculosis: a molecular epidemiological surveillance study. Lancet Microbe. doi:10.1016/S2666-5247(20)30038-0
- Dawson KL, Bell A, Kawakami RP (2012). Transmission of ( complex species) from a tuberculosis patient to a dairy cow in New Zealand. J Clin Microbiol. doi:10.1128/JCM.01652-12
- Marcos LA, Spitzer ED, Mahapatra R (2017). Lymphadenitis in New York, USA. Emerg Infect Dis. doi:10.3201/eid2310.170490
- Lipworth SIW, Jajou R, de Neeling H (2017). A novel multi SNP based method for the identification of subspecies and associated lineages and sub-lineages of the Mycobacterium tuberculosis complex by whole genome sequencing. bioRxiv. doi:10.1101/213850
- Lavender CJ, Globan M, Kelly H (2013). Epidemiology and control of tuberculosis in Victoria, a low-burden state in south-eastern Australia, 2005-2010. Int J Tuberc Lung Dis. doi:10.5588/ijtld.12.0791
- Allix-Béguec C, Arandjelovic I (2018). Prediction of Susceptibility to First-Line Tuberculosis Drugs by DNA Sequencing. N Engl J Med. doi:10.1056/NEJMoa1800474
- Riojas MA, McGough KJ, Rider-Riojas CJ (2018). Phylogenomic analysis of the species of the complex demonstrates that and are later heterotypic synonyms of. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.002507
- Cohan FM (2006). Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philos Trans R Soc Lond B Biol Sci. doi:10.1098/rstb.2006.1918
- Smith NH, Kremer K, Inwald J (2006). Ecotypes of the complex. J Theor Biol. doi:10.1016/j.jtbi.2005.08.036
- Marianelli C, Amato B, Boniotti MB (2019). Genotype diversity and distribution of from livestock in a small, high-risk area in northeastern Sicily, Italy. PLoS Negl Trop Dis. doi:10.1371/journal.pntd.0007546
- Ghielmetti G, Scherrer S, Friedel U (2017). Epidemiological tracing of bovine tuberculosis in Switzerland, multilocus variable number of tandem repeat analysis of and. PLoS One. doi:10.1371/journal.pone.0172474
- Almaw G, Mekonnen GA, Mihret A (2021). Population structure and transmission of in Ethiopia. Microb Genom. doi:10.1099/mgen.0.000539
- Katale BZ, Mbelele PM, Lema NA (2020). Whole genome sequencing of isolates and clinical outcomes of patients treated for multidrug-resistant tuberculosis in Tanzania. BMC Genomics. doi:10.1186/s12864-020-6577-1
- Rosenthal A, Gabrielian A, Engle E (2017). The TB Portals: an Open-Access, Web-Based Platform for Global Drug-Resistant-Tuberculosis Data Sharing and Analysis. J Clin Microbiol. doi:10.1128/JCM.01013-17
- Beckert P, Sanchez-Padilla E, Merker M (2020). MDR outbreak clone in Eswatini missed by Xpert has elevated bedaquiline resistance dated to the pre-treatment era. Genome Med. doi:10.1186/s13073-020-00793-8
- Ciaravino G, Vidal E, Cortey M (2021). Phylogenetic relationships investigation of strains from sympatric wild boar and goats based on whole genome sequencing. Transbound Emerg Dis. doi:10.1111/tbed.13816
- Belisle JT, Sonnenberg MG (1998). Isolation of genomic DNA from mycobacteria. Methods Mol Biol. doi:10.1385/0-89603-471-2:31
- Menardo F, Loiseau C, Brites D (2018). Treemmer: a tool to reduce large phylogenetic datasets with minimal loss of diversity. BMC Bioinformatics. doi:10.1186/s12859-018-2164-8
- Bolger AM, Lohse M, Usadel B (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. doi:10.1093/bioinformatics/btu170
- Li H, Handsaker B, Wysoker A (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics. doi:10.1093/bioinformatics/btp352
- Comas I, Chakravartti J, Small PM (2010). Human T cell epitopes of are evolutionarily hyperconserved. Nat Genet. doi:10.1038/ng.590
- McKenna A, Hanna M, Banks E (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. doi:10.1101/gr.107524.110
- Li H (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. doi:10.1093/bioinformatics/btr509
- Koboldt DC, Zhang Q, Larson DE (2012). VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. doi:10.1101/gr.129684.111
- Garnier T, Eiglmeier K, Camus JC (2003). The complete genome sequence of . Proc Natl Acad Sci U S A. doi:10.1073/pnas.1130426100
- Cingolani P, Platts A, Wang le L (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: . Fly (Austin). doi:10.4161/fly.19695
- Stucki D, Brites D, Jeljeli L (2016). lineage 4 comprises globally distributed and geographically restricted sublineages. Nat Genet. doi:10.1038/ng.3704
- Steiner A, Stucki D, Coscolla M (2014). KvarQ: targeted and direct variant calling from fastq reads of bacterial genomes. BMC Genomics. doi:10.1186/1471-2164-15-881
- Stamatakis A (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. doi:10.1093/bioinformatics/btu033
- Yu G, Smith DK, Zhu H (2017). ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. doi:10.1111/2041-210X.12628
- Jombart T (2008). : a R package for the multivariate analysis of genetic markers. Bioinformatics. doi:10.1093/bioinformatics/btn129
- Paradis E, Claude J, Strimmer K (2004). APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. doi:10.1093/bioinformatics/btg412
- South A (2011). rworldmap: A New R package for Mapping Global Data. The R Journal. doi:10.32614/RJ-2011-006
- (2018). R: A Language and Environment for Statistical Computing.
- Danecek P, Auton A, Abecasis G (2011). The variant call format and VCFtools. Bioinformatics. doi:10.1093/bioinformatics/btr330
- Obenchain V, Lawrence M, Carey V (2014). VariantAnnotation: a Bioconductor package for exploration and annotation of genetic variants. Bioinformatics. doi:10.1093/bioinformatics/btu168
- (2021). dbrites/LivestockAssociatedMTBC: (1.1.0). Zenodo.
- Carneiro PA, Zimpel CK, Pasquatti TN (2021). Genetic Diversity and Potential Paths of Transmission of in the Amazon: The Discovery of M. bovis Lineage Lb1 Circulating in South America. Front Vet Sci. doi:10.3389/fvets.2021.630989
- Rodrigues RA, Ribeiro Araujo F, Rivera Davila AM (2021). Genomic and temporal analyses of in southern Brazil. Microb Genom. doi:10.1099/mgen.0.000569
- Tazerart F, Saad J, Sahraoui N (2021). Whole Genome Sequence Analysis of Cattle Isolates, Algeria. Pathogens. doi:10.3390/pathogens10070802
- Brosch R, Gordon SV, Marmiesse M (2002). A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A. doi:10.1073/pnas.052548299
- Salvador LCM, O'Brien DJ, Cosgrove MK (2019). Disease management at the wildlife-livestock interface: Using whole-genome sequencing to study the role of elk in transmission in Michigan, USA. Mol Ecol. doi:10.1111/mec.15061
- Crispell J, Zadoks RN, Harris SR (2017). Using whole genome sequencing to investigate transmission in a multi-host system: bovine tuberculosis in New Zealand. BMC Genomics. doi:10.1186/s12864-017-3569-x
- Crispell J, Benton CH, Balaz D (2019). Combining genomics and epidemiology to analyse bi-directional transmission of in a multi-host system. Elife. doi:10.7554/eLife.45833
- Oloya J, Kazwala R, Lund A (2007). Characterisation of mycobacteria isolated from slaughter cattle in pastoral regions of Uganda. BMC Microbiol. doi:10.1186/1471-2180-7-95
- Clifford DL, Kazwala RR, Sadiki H (2013). Tuberculosis infection in wildlife from the Ruaha ecosystem Tanzania: implications for wildlife, domestic animals, and human health. Epidemiol Infect. doi:10.1017/S0950268813000836
- Fitzgerald SD, Kaneene JB (2013). Wildlife reservoirs of bovine tuberculosis worldwide: hosts, pathology, surveillance, and control. Vet Pathol. doi:10.1177/0300985812467472
- Price-Carter M, Brauning R, de Lisle GW (2018). Whole Genome Sequencing for Determining the Source of Infections in Livestock Herds and Wildlife in New Zealand. Front Vet Sci. doi:10.3389/fvets.2018.00272
- Zimpel CK, Brandao PE, de Souza Filho AF (2017). Complete Genome Sequencing of SP38 and Comparative Genomics of and Strains. Front Microbiol. doi:10.3389/fmicb.2017.02389
- Rodriguez S, Bezos J, Romero B (2011). Mycobacterium caprae infection in livestock and wildlife, Spain. Emerg Infect Dis. doi:10.3201/eid1703.100618
- Orlowska B, Krajewska-Wedzina M, Augustynowicz-Kopec E (2020). Epidemiological characterization of Mycobacterium caprae strains isolated from wildlife in the Bieszczady Mountains, on the border of Southeast Poland. BMC Vet Res. doi:10.1186/s12917-020-02581-3
- Broeckl S, Krebs S, Varadharajan A (2017). Investigation of intra-herd spread of Mycobacterium caprae in cattle by generation and use of a whole-genome sequence. Vet Res Commun. doi:10.1007/s11259-017-9679-8
- Prodinger WM, Indra A, Koksalan OK (2014). infection in humans. Expert Rev Anti Infect Ther. doi:10.1586/14787210.2014.974560
- Kubica T, Rusch-Gerdes S, Niemann S (2003). subsp. caused one-third of human -associated tuberculosis cases reported in Germany between 1999 and 2001. J Clin Microbiol. doi:10.1128/JCM.41.7.3070-3077.2003
- Domogalla J, Prodinger WM, Blum H (2013). Region of difference 4 in alpine isolates indicates three variants. J Clin Microbiol. doi:10.1128/JCM.02966-12
- Zignol M, Cabibbe AM, Dean AS (2018). Genetic sequencing for surveillance of drug resistance in tuberculosis in highly endemic countries: a multi-country population-based surveillance study. Lancet Infect Dis. doi:10.1016/S1473-3099(18)30073-2
- Parsons SDC (2020). : a zoonosis, zooanthroponosis, or both?. Lancet Microbe. doi:10.1016/S2666-5247(20)30145-2
- Refaya AK, Bhargavi G, Mathew NC (2020). A review on bovine tuberculosis in India. Tuberculosis (Edinb). doi:10.1016/j.tube.2020.101923
- Muller B, Durr S, Alonso S (2013). Zoonotic -induced tuberculosis in humans. Emerg Infect Dis. doi:10.3201/eid1906.120543
- Branger M, Loux V, Cochard T (2020). The complete genome sequence of Mb3601, a SB0120 spoligotype strain representative of a new clonal group. Infect Genet Evol. doi:10.1016/j.meegid.2020.104309
- Oettinger T, Jørgensen M, Ladefoged A (1999). Development of the BCG vaccine: review of the historical and biochemical evidence for a genealogical tree. Tuber Lung Dis. doi:10.1054/tuld.1999.0206
- Çavuşoğlu C, Yilmaz FF (2017). Molecular Epidemiology of Human Infection in Aegean Region, Turkey. Mikrobiyol Bul. doi:10.5578/mb.53963
- Koni A, Tafaj S, Loda D (2018). Genotyping and spoligotyping of isolates from positive tuberculin skin test cattle in Albania. Albanian J Agric Sci.
- Berg S, Firdessa R, Habtamu M (2009). The burden of mycobacterial disease in ethiopian cattle: implications for public health. PLoS One. doi:10.1371/journal.pone.0005068
- Phelan JE, O'Sullivan DM, Machado D (2019). Integrating informatics tools and portable sequencing technology for rapid detection of resistance to anti-tuberculous drugs. Genome Med. doi:10.1186/s13073-019-0650-x
- Brites D (2021). A new nomenclature for the livestock-associated Mycobacterium tuberculosis complex based on phylogenomics.