Phylogenomics of Mycobacterium africanum reveals a new lineage and a complex evolutionary history

Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M. tuberculosis sensu stricto , as well as two lineages (L5 and L6) traditionally referred to as Mycobacterium africanum . Strains of L5 and L6 ar...

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Published inMicrobial genomics Vol. 7; no. 2
Main Authors Coscolla, Mireia, Gagneux, Sebastien, Menardo, Fabrizio, Loiseau, Chloé, Ruiz-Rodriguez, Paula, Borrell, Sonia, Otchere, Isaac Darko, Asante-Poku, Adwoa, Asare, Prince, Sánchez-Busó, Leonor, Gehre, Florian, Sanoussi, C. N’Dira, Antonio, Martin, Affolabi, Dissou, Fyfe, Janet, Beckert, Patrick, Niemann, Stefan, Alabi, Abraham S., Grobusch, Martin P., Kobbe, Robin, Parkhill, Julian, Beisel, Christian, Fenner, Lukas, Böttger, Erik C., Meehan, Conor J., Harris, Simon R., de Jong, Bouke C., Yeboah-Manu, Dorothy, Brites, Daniela
Format Journal Article
LanguageEnglish
Published England Microbiology Society 01.02.2021
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Abstract Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M. tuberculosis sensu stricto , as well as two lineages (L5 and L6) traditionally referred to as Mycobacterium africanum . Strains of L5 and L6 are largely limited to West Africa for reasons unknown, and little is known of their genomic diversity, phylogeography and evolution. Here, we analysed the genomes of 350 L5 and 320 L6 strains, isolated from patients from 21 African countries, plus 5 related genomes that had not been classified into any of the known MTBC lineages. Our population genomic and phylogeographical analyses showed that the unclassified genomes belonged to a new group that we propose to name MTBC lineage 9 (L9). While the most likely ancestral distribution of L9 was predicted to be East Africa, the most likely ancestral distribution for both L5 and L6 was the Eastern part of West Africa. Moreover, we found important differences between L5 and L6 strains with respect to their phylogeographical substructure and genetic diversity. Finally, we could not confirm the previous association of drug-resistance markers with lineage and sublineages. Instead, our results indicate that the association of drug resistance with lineage is most likely driven by sample bias or geography. In conclusion, our study sheds new light onto the genomic diversity and evolutionary history of M. africanum , and highlights the need to consider the particularities of each MTBC lineage for understanding the ecology and epidemiology of TB in Africa and globally.
AbstractList Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M. tuberculosis sensu stricto , as well as two lineages (L5 and L6) traditionally referred to as Mycobacterium africanum . Strains of L5 and L6 are largely limited to West Africa for reasons unknown, and little is known of their genomic diversity, phylogeography and evolution. Here, we analysed the genomes of 350 L5 and 320 L6 strains, isolated from patients from 21 African countries, plus 5 related genomes that had not been classified into any of the known MTBC lineages. Our population genomic and phylogeographical analyses showed that the unclassified genomes belonged to a new group that we propose to name MTBC lineage 9 (L9). While the most likely ancestral distribution of L9 was predicted to be East Africa, the most likely ancestral distribution for both L5 and L6 was the Eastern part of West Africa. Moreover, we found important differences between L5 and L6 strains with respect to their phylogeographical substructure and genetic diversity. Finally, we could not confirm the previous association of drug-resistance markers with lineage and sublineages. Instead, our results indicate that the association of drug resistance with lineage is most likely driven by sample bias or geography. In conclusion, our study sheds new light onto the genomic diversity and evolutionary history of M. africanum , and highlights the need to consider the particularities of each MTBC lineage for understanding the ecology and epidemiology of TB in Africa and globally.
Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M. tuberculosis sensu stricto, as well as two lineages (L5 and L6) traditionally referred to as Mycobacterium africanum. Strains of L5 and L6 are largely limited to West Africa for reasons unknown, and little is known of their genomic diversity, phylogeography and evolution. Here, we analysed the genomes of 350 L5 and 320 L6 strains, isolated from patients from 21 African countries, plus 5 related genomes that had not been classified into any of the known MTBC lineages. Our population genomic and phylogeographical analyses showed that the unclassified genomes belonged to a new group that we propose to name MTBC lineage 9 (L9). While the most likely ancestral distribution of L9 was predicted to be East Africa, the most likely ancestral distribution for both L5 and L6 was the Eastern part of West Africa. Moreover, we found important differences between L5 and L6 strains with respect to their phylogeographical substructure and genetic diversity. Finally, we could not confirm the previous association of drug-resistance markers with lineage and sublineages. Instead, our results indicate that the association of drug resistance with lineage is most likely driven by sample bias or geography. In conclusion, our study sheds new light onto the genomic diversity and evolutionary history of M. africanum, and highlights the need to consider the particularities of each MTBC lineage for understanding the ecology and epidemiology of TB in Africa and globally.Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M. tuberculosis sensu stricto, as well as two lineages (L5 and L6) traditionally referred to as Mycobacterium africanum. Strains of L5 and L6 are largely limited to West Africa for reasons unknown, and little is known of their genomic diversity, phylogeography and evolution. Here, we analysed the genomes of 350 L5 and 320 L6 strains, isolated from patients from 21 African countries, plus 5 related genomes that had not been classified into any of the known MTBC lineages. Our population genomic and phylogeographical analyses showed that the unclassified genomes belonged to a new group that we propose to name MTBC lineage 9 (L9). While the most likely ancestral distribution of L9 was predicted to be East Africa, the most likely ancestral distribution for both L5 and L6 was the Eastern part of West Africa. Moreover, we found important differences between L5 and L6 strains with respect to their phylogeographical substructure and genetic diversity. Finally, we could not confirm the previous association of drug-resistance markers with lineage and sublineages. Instead, our results indicate that the association of drug resistance with lineage is most likely driven by sample bias or geography. In conclusion, our study sheds new light onto the genomic diversity and evolutionary history of M. africanum, and highlights the need to consider the particularities of each MTBC lineage for understanding the ecology and epidemiology of TB in Africa and globally.
Human tuberculosis (TB) is caused by members of the complex (MTBC). The MTBC comprises several human-adapted lineages known as , as well as two lineages (L5 and L6) traditionally referred to as . Strains of L5 and L6 are largely limited to West Africa for reasons unknown, and little is known of their genomic diversity, phylogeography and evolution. Here, we analysed the genomes of 350 L5 and 320 L6 strains, isolated from patients from 21 African countries, plus 5 related genomes that had not been classified into any of the known MTBC lineages. Our population genomic and phylogeographical analyses showed that the unclassified genomes belonged to a new group that we propose to name MTBC lineage 9 (L9). While the most likely ancestral distribution of L9 was predicted to be East Africa, the most likely ancestral distribution for both L5 and L6 was the Eastern part of West Africa. Moreover, we found important differences between L5 and L6 strains with respect to their phylogeographical substructure and genetic diversity. Finally, we could not confirm the previous association of drug-resistance markers with lineage and sublineages. Instead, our results indicate that the association of drug resistance with lineage is most likely driven by sample bias or geography. In conclusion, our study sheds new light onto the genomic diversity and evolutionary history of , and highlights the need to consider the particularities of each MTBC lineage for understanding the ecology and epidemiology of TB in Africa and globally.
Author Grobusch, Martin P.
Fenner, Lukas
Yeboah-Manu, Dorothy
Otchere, Isaac Darko
Borrell, Sonia
Alabi, Abraham S.
Affolabi, Dissou
Fyfe, Janet
Beisel, Christian
Gagneux, Sebastien
Sanoussi, C. N’Dira
Coscolla, Mireia
Beckert, Patrick
Kobbe, Robin
Gehre, Florian
Harris, Simon R.
de Jong, Bouke C.
Loiseau, Chloé
Menardo, Fabrizio
Ruiz-Rodriguez, Paula
Parkhill, Julian
Meehan, Conor J.
Sánchez-Busó, Leonor
Niemann, Stefan
Asante-Poku, Adwoa
Böttger, Erik C.
Brites, Daniela
Asare, Prince
Antonio, Martin
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33555243$$D View this record in MEDLINE/PubMed
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Issue 2
Keywords genome
diversity
evolution
Mycobacterium tuberculosis
mycobacteria
Mycobacterium africanum
Language English
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All raw data generated for this study have been submitted to the European Nucleotide Archive (ENA; https://www.ebi.ac.uk/ena/) under the study accession numbers PRJEB9003, PRJEB38656, PRJEB4884, PRJEB38317, PRJEB31139, PRJEB6273 and PRJEB31144. Individual run accession numbers for new and published sequences are indicated in Table S1.
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0000-0002-4162-0228
0000-0002-8090-2287
0000-0002-1663-6287
0000-0003-0673-5967
0000-0002-7885-4482
0000-0003-0727-5974
0000-0001-8929-193X
0000-0003-0724-8343
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PublicationTitle Microbial genomics
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Snippet Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M....
Human tuberculosis (TB) is caused by members of the complex (MTBC). The MTBC comprises several human-adapted lineages known as , as well as two lineages (L5...
Human tuberculosis (TB) is caused by members of the Mycobacterium tuberculosis complex (MTBC). The MTBC comprises several human-adapted lineages known as M....
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SubjectTerms Africa, Eastern
Africa, Western
Drug Resistance, Bacterial
Evolution, Molecular
Genome, Bacterial
High-Throughput Nucleotide Sequencing
Humans
Mycobacterium tuberculosis - classification
Mycobacterium tuberculosis - genetics
Mycobacterium tuberculosis - isolation & purification
Phylogeny
Phylogeography
Tuberculosis - microbiology
Whole Genome Sequencing - methods
Title Phylogenomics of Mycobacterium africanum reveals a new lineage and a complex evolutionary history
URI https://www.ncbi.nlm.nih.gov/pubmed/33555243
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https://pubmed.ncbi.nlm.nih.gov/PMC8208692
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