Phylogenomic Perspective on a Unique Mycobacterium bovis Clade Dominating Bovine Tuberculosis Infections among Cattle and Buffalos in Northern Brazil

Conceição, Marília Lima da; Conceição, Emilyn Costa; Furlaneto, Ismari Perini; Silva, Sandro Patroca da; Guimarães, Arthur Emil Dos Santos; Gomes, Pedro; Boschiroli, María Laura; Michelet, Lorraine; Kohl, Thomas A.; Kranzer, Katharina; Francez, Loreno da Costa; Lima, Luana Nepomuceno Gondim Costa; Portugal, Isabel; Perdigão, João; Lima, Karla Valéria Batista

doi:10.1038/s41598-020-58398-5

Cited by 11 publications

(31 citation statements)

References 45 publications

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“…Maximum likelihood (ML) phylogenetic tree from concatenated SNPs (single nucleotide polymorphisms) of Mycobacterium bovis genomes sequenced in this study and by Conceição et al ( 24 ) from Marajó Island. Blue tips: M. bovis genomes obtained from cattle and sequenced in this study; red tips: M. bovis genomes obtained from buffalo and sequenced in this study; green tips: M. bovis genomes from unknown hosts sequenced by Conceição et al ( 24 ) and obtained from cattle or buffalo from Marajó Island, Pará; black tips: Mycobacterium caprae genomes (outgroup). Purple bar, M. bovis genomes carrying markers of European 2 clonal complex; gray bar, M. bovis genomes carrying no markers of known clonal complexes.…”

Section: Resultsmentioning

confidence: 93%

“…As to evaluate genetic diversity of M. bovis in the geographic region, 15 quality-approved M. bovis genomes previously sequenced and obtained from cattle and buffalo of the Marajó Island ( 24 ) (ENA accession number ERP116404 ) were used to evaluate the phylogenetic relatedness with the M. bovis genomes sequenced in this study. The Marajó Island is geographically close to the targeted region analyzed herein ( Figure 1 ), together with the Lower Amazon River Basin are the regions of major concentration of bufallo in the country, and these M. bovis genomes ( 24 ) were the only strains of the North of Brazil sequenced up until this study. These genomes were quality-assessed and SNPs were obtained as described above.…”

Section: Methodsmentioning

confidence: 99%

“…Mycobacterium bovis genomes obtained from this study and those from Marajó Island ( 24 ) were compared against a collection of 106 genomes representing the four M. bovis lineages (Lb1–Lb4) and unknown groups 1, 2, and 3 from a recent study that evaluated worldwide distribution and evolution of M. bovis genomes ( 9 ) ( Supplementary Data Sheet 1 ). In addition, 21 quality-approved M. bovis genomes from France ( 39 ), which include representatives of the recently suggested CC called European 3 ( 40 ), were also included in the analysis ( Supplementary Data Sheet 1 ).…”

Section: Methodsmentioning

confidence: 99%

“…In addition, the knowledge regarding strain diversity within host species has special contribution in areas under risk of zoonotic TB occurrence, thereby providing new insights in strain distribution that may help establishing strategic measures for TB control and prevention ( 18 , 19 ). In Brazil, few and dispersed molecular epidemiologic studies of M. bovis have been reported ( 20 – 24 ), and the WGS characterization of the pathogen is just starting to be unraveled ( 24 – 26 ). While few studies focused on areas of high dairy herd productivity ( 25 , 26 ), a recent study evaluating M. bovis genomes obtained from buffalo and cattle of the Marajó Island, Northern Brazil, was performed and showed the existence of a monophyletic group without CC classification ( 24 ).…”

Section: Introductionmentioning

confidence: 99%

“…In Brazil, few and dispersed molecular epidemiologic studies of M. bovis have been reported ( 20 – 24 ), and the WGS characterization of the pathogen is just starting to be unraveled ( 24 – 26 ). While few studies focused on areas of high dairy herd productivity ( 25 , 26 ), a recent study evaluating M. bovis genomes obtained from buffalo and cattle of the Marajó Island, Northern Brazil, was performed and showed the existence of a monophyletic group without CC classification ( 24 ). Therefore, the aim of this study was to apply whole-genome and SNP-based phylogenomic analyses to obtain novel information regarding the genetic diversity of M. bovis strains circulating in buffalo and cattle from the region of the Lower Amazon River Basin.…”

Section: Introductionmentioning

confidence: 99%

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Genetic Diversity and Potential Paths of Transmission of Mycobacterium bovis in the Amazon: The Discovery of M. bovis Lineage Lb1 Circulating in South America

et al. 2021

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Bovine tuberculosis (bTB) has yet to be eradicated in Brazil. Herds of cattle and buffalo are important sources of revenue to people living in the banks of the Amazon River basin. A better understanding of Mycobacterium bovis (M. bovis) populational structure and transmission dynamics affecting these animals can significantly contribute in efforts to improve their sanitary status. Herein, we sequenced the whole genome of 22 M. bovis isolates (15 from buffalo and 7 from cattle) from 10 municipalities in the region of the Lower Amazon River Basin in Brazil and performed phylogenomic analysis and Single Nucleotide Polymorphism (SNP)-based transmission inference to evaluate population structure and transmission networks. Additionally, we compared these genomes to others obtained in unrelated studies in the Marajó Island (n = 15) and worldwide (n = 128) to understand strain diversity in the Amazon and to infer M. bovis lineages. Our results show a higher genomic diversity of M. bovis genomes obtained in the Lower Amazon River region when compared to the Marajó Island, while no significant difference was observed between M. bovis genomes obtained from cattle and buffalo (p ≥ 0.05). This high genetic diversity is reflected by the weak phylogenetic clustering of M. bovis from the Lower Amazon River region based on geographic proximity and in the detection of only two putative transmission clusters in the region. One of these clusters is the first description of inter-species transmission between cattle and buffalo in the Amazon, bringing implications to the bTB control program. Surprisingly, two M. bovis lineages were detected in our dataset, namely Lb1 and Lb3, constituting the first description of Lb1 in South America. Most of the strains of this study (13/22) and all 15 strains of the Marajó Island carried no clonal complex marker, suggesting that the recent lineage classification better describe the diversity of M. bovis in the Amazon.

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Section: Resultsmentioning

confidence: 93%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Genetic Diversity and Potential Paths of Transmission of Mycobacterium bovis in the Amazon: The Discovery of M. bovis Lineage Lb1 Circulating in South America

et al. 2021

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Genomic and temporal analyses of Mycobacterium bovis in southern Brazil

et al. 2021

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Mycobacterium bovis is a causal agent of bovine tuberculosis (bTB), one of the most important diseases currently facing the cattle industry worldwide. Tracing the source of M. bovis infections of livestock is an important tool for understanding the epidemiology of bTB and defining control/eradication strategies. In this study, whole genome sequencing (WGS) of 74 M . bovis isolates sourced from naturally infected cattle in the State of Rio Grande do Sul (RS), southern Brazil, was used to evaluate the population structure of M. bovis in the region, identify potential transmission events and date the introduction of clonal complex (CC) European 2 (Eu2). In silico spoligotyping identified 11 distinct patterns including four new profiles and two CCs, European 1 (Eu1) and Eu2. The analyses revealed a high level of genetic diversity in the majority of herds and identified putative transmission clusters that suggested that within- and between-herd transmission is occurring in RS. In addition, a comparison with other published M. bovis isolates from Argentina, Brazil, Paraguay and Uruguay demonstrated some evidence for a possible cross-border transmission of CC Eu1 into RS from Uruguay or Argentina. An estimated date for the introduction of CC Eu2 into RS in the middle of the 19th century correlated with the historical introduction of cattle into RS to improve existing local breeds. These findings contribute to the understanding of the population structure of M. bovis in southern Brazil and highlight the potential of WGS in surveillance and helping to identify bTB transmission.

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A new nomenclature for the livestock-associated Mycobacterium tuberculosis complex based on phylogenomics

Zwyer¹,

Çavuşoğlu²,

Ghielmetti³

et al. 2021

Open Res Europe

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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 8,747 whole-genome sequences (WGS) from public sources and 39 newly sequenced strains, and selected a subset of 839 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 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 makers were implemented in a new test suit in KvarQ, a platform-independent, open-source tool. 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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Phylogenomic Perspective on a Unique Mycobacterium bovis Clade Dominating Bovine Tuberculosis Infections among Cattle and Buffalos in Northern Brazil

Cited by 11 publications

References 45 publications

Genetic Diversity and Potential Paths of Transmission of Mycobacterium bovis in the Amazon: The Discovery of M. bovis Lineage Lb1 Circulating in South America

Genetic Diversity and Potential Paths of Transmission of Mycobacterium bovis in the Amazon: The Discovery of M. bovis Lineage Lb1 Circulating in South America

Genomic and temporal analyses of Mycobacterium bovis in southern Brazil

A new nomenclature for the livestock-associated Mycobacterium tuberculosis complex based on phylogenomics

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