Turkish and Japanese Mycobacterium tuberculosis sublineages share a remote common ancestor

Refrégier, Guislaine; Abadia, Edgar; Matsumoto, Tomoshige; Ano, Hiromi; Takashima, Tetsuya; Tsuyuguchi, Izuo; Aktaş, Elif; Cömert, Füsun; Gomgnimbou, Michel K.; Panaiotov, Stefan; Phelan, Jody; Coll, Francesc Español i; McNerney, Ruth; Pain, Arnab; Clark, Taane G.; Sola, Christophe

doi:10.1016/j.meegid.2016.10.009

Cited by 9 publications

(7 citation statements)

References 66 publications

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“…For example, RD-Rio sublineage within the Latin American Mediterranean family could have originated in West Africa but its epidemic circulation and primary dispersal started in Brazil [ 12 ]. Thus the Ural family was estimated to originate in the area north of the Black Sea > 1800 years ago [ 4 , 5 , 13 ] and this dating seems at odds with our estimation of 150–300 years ago. However only a single strain with prototype Ural spoligotype SIT777 was available in the studied dataset and consequently the estimated time is TMRCA of the currently circulating and derived clades, Clade A (SIT35) and Clades B and C (SIT262).…”

Section: Discussioncontrasting

confidence: 71%

New epidemic cluster of pre-extensively drug resistant isolates of Mycobacterium tuberculosis Ural family emerging in Eastern Europe

et al. 2018

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BackgroundUral genetic family is a part of the Euro-American lineage of Mycobacterium tuberculosis and is endemic in Northern Eurasia (former Soviet Union [FSU]). These strains were long described as drug susceptible and of low virulence, but recent studies reported an increasing circulation of the multidrug-resistant (MDR) and extensively drug-resistant (XDR) Ural strains. Here, we analyzed all publicly available whole genome sequence data of Ural genotype isolates, in order to elucidate their phylogenomic diversity with a special focus on MDR and potentially epidemic clones.ResultsA total of 149 M. tuberculosis genomes of Ural isolates from FSU countries were mined from the GMTV database and TB-ARC project. We identified 6002 variable amino acid positions that were assessed for functional significance and used to build ML, NJ trees and for Bayesian TMRCA estimation. Three robust monophyletic clades were identified: Clade A (31 isolates from Russia, Belarus, Moldova), Clade B (52 isolates from Russia), and Clade C (37 isolates from Moldova, 2 from Belarus). Clade C was significantly associated with XDR or pre-XDR status compared to the pooled Clades A and B (33/39 versus 5/83, P < 0.0001). Time of origin was estimated for Clade A at 77.7–137 years ago and for Clade B at 56.3–99.2 years ago compared to the significantly more recent origin for Clade C. in silico spoligotyping identified signatures specific of the Clade A (spoligotype SIT35), and Clades B and C (both SIT262).ConclusionsA genetically compact and evolutionarily young Ural Clade C, likely originated after collapse of the Soviet Union, and reached epidemic proportions in Moldova in the last 20 years. This epidemic pre-XDR clone (mostly rifampin, isoniazid and kanamycin resistant) is characterized by a specific combination of mutations: KatG Ser315Thr, fabG1 -15C > T, RpoB Ser450Leu, RpsL Lys88Arg, eis -12G > A and EmbB Ser297Ala/T > G. Its further dissemination may occur towards both Russia and European Union and should be taken into consideration by health authorities. The identified spoligotyping signatures can serve for rapid preliminary detection and surveillance of the more hazardous pre-XDR associated strains of the Ural family, both in populations from countries of their endemic circulation and migrant communities.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5162-3) contains supplementary material, which is available to authorized users.

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Section: Discussioncontrasting

confidence: 71%

New epidemic cluster of pre-extensively drug resistant isolates of Mycobacterium tuberculosis Ural family emerging in Eastern Europe

et al. 2018

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“…Our study confirms that L4.6.2 is spread over the whole country. Further whole genome sequencing (WGS) would also allow to estimate divergence times and phylogeny within and between sublineages by estimating molecular clock rates based on single nucleotide polymorphisms (SNPs) numbers detected [ 30 , 31 ].…”

Section: Discussionmentioning

confidence: 99%

Mycobacterium tuberculosis complex genotypes circulating in Nigeria based on spoligotyping obtained from Ziehl-Neelsen stained slides extracted DNA

et al. 2018

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Tuberculosis (TB) remains one of the most threatening diseases and Nigeria has one of the world’s largest burdens. This study performed high-throughput spoligotyping directly on sputum smears to describe the Mycobacterium tuberculosis strains circulating among new TB patients in Nigeria.MethodsAll State TB control programmes in Nigeria were requested to submit 25–50 smear-positive Ziehl-Neelsen (ZN) stained slides for screening during 2013–2014. DNA was extracted from 929 slides for spoligotyping and drug-resistance analysis using microbead-based flow-cytometry suspension arrays.ResultsSpoligotyping results were obtained for 549 (59.1%) of 929 samples. Lineage 4 Cameroon sublineage (L4.6.2) represented half of the patterns, Mycobacterium africanum (L5 and L6) represented one fifth of the patterns, and all other lineages, including other L4 sublineages, represented one third of the patterns. Sublineage L4.6.2 was mostly identified in the north of the country whereas L5 was mostly observed in the south and L6 was scattered. The spatial distribution of genotypes had genetic geographic gradients. We did not obtain results enabling the detection of drug-resistance mutations.Conclusion/SignificanceWe present the first national snapshot of the M. tuberculosis spoligotypes circulating in Nigeria based on ZN slides. Spoligotyping data can be obtained in a rapid and high-throughput manner with DNA extracted from ZN-stained slides, which may potentially improve our understanding of the genetic epidemiology of TB.

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“…Dating of strains diversification is important to identify the conditions that fostered past epidemics. Here, according to consensus molecular clock of TB on the middle term, the time frame of coalescence of AAnc5 sublineage landmarks could be between 280-310 years ago before present for the closest isolates, and 760-800 years ago for the farthest ones [73].…”

Section: Discussionmentioning

confidence: 99%

“…Dating can be comforted if adequate correlation exists between historical, genomic, epidemiological and demographic facts. In a former similar study, three scenarios have been tested for the dating of a L4.2 sublineage occurring in Japan and Turkey using historical, anthropological, human genetics, paleopathological events and genomics [73].…”

Section: Discussionmentioning

confidence: 99%

“…Islands are indeed excellent settings to distinguish endemic from imported species and tuberculosis history, as all infectious diseases, is definitively linked to human migration and local and global demographic history [107]. Since Japan is now a country with a very low tuberculosis prevalence rate (13 per 100,000 in 2017), it is an excellent setting to try to identify the historical events linked to past tuberculosis outbreaks [73].…”

Section: Discussionmentioning

confidence: 99%

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Connection between two historical tuberculosis outbreak sites in Japan, Honshu, due to a new ancestral L2 sublineage

Guyeux

Senelle

Refrégier

et al. 2021

Preprint

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By gathering an initial collection of 680 public Sequence Read Archives from the Mycobacterium tuberculosis complex (MTC) including 190 belonging to the lineage 2 Beijing, and using a new bioinformatical pipeline, TB-Annotator, that analyzes more than 50,000 characters, we characterized a phylogenetically significant L2 sublineage from isolates found in Tochigi province, that we designate as Asia Ancestral 5. These isolates harbor a number of specific criteria (42 specific SNPs) and their intra-cluster pairwise distance suggested historical and not epidemiological transmission. These isolates harbor a mutation in rpoC, and do not fulfill, either the Modern Beijing lineage criteria (L2.2.1.2.2) or the other currently known Ancestral Beijing lineages described so far. Asia Ancestral 5 isolates do not possess mutT2 58 and ogt 12 characteristics of Modern Beijing, but possess ancient evolutionary characteristics. By looking into the literature, we found in a reference isolate ID381, found in Kobe and Osaka, and defined as G3, 36 out of 42 shared and specific SNPs in the same sublineage. Using this study, we also confirmed the intermediate position of the Asia Ancestral 4 recently described in Thailand and suggest an improved classification of the L2 that now includes Asia Ancestral 4 and 5. Increasing the recruitment to around 3000 genomes (including 642 belonging to L2) confirmed our results and suggest new historical ancestral L2 phylogenetically relevant branches that remain to be investigated in detail. We discuss some anthropological and historical data from Japan history and its link to Korea and China. This study shows that the reconstruction of the early history of tuberculosis pandemia in Asia is likely to reveal complex patterns since its emergence.

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Turkish and Japanese Mycobacterium tuberculosis sublineages share a remote common ancestor

Cited by 9 publications

References 66 publications

New epidemic cluster of pre-extensively drug resistant isolates of Mycobacterium tuberculosis Ural family emerging in Eastern Europe

New epidemic cluster of pre-extensively drug resistant isolates of Mycobacterium tuberculosis Ural family emerging in Eastern Europe

Mycobacterium tuberculosis complex genotypes circulating in Nigeria based on spoligotyping obtained from Ziehl-Neelsen stained slides extracted DNA

Connection between two historical tuberculosis outbreak sites in Japan, Honshu, due to a new ancestral L2 sublineage

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