Insights into Population Genetics and Phylogeography of Mycobacterium tuberculosis
https://doi.org/10.58838/2075-1230-2024-102-5-91-98
Abstract
The review summarizes the current understanding of population genetics and genetic classification of Mycobacterium tuberculosis. Articles accumulated in Elibrary and PubMed were used as a source of information. Using keywords, more than 100 publications were found and analyzed for the period from 2009 to 2023, 35 of which were included in the review. According to the current concept, M. tuberculosis is represented by nine lineages (superfamilies L1-L9), each of which has different characteristics of evolutionary status, genetic diversity, transmissibility, drug resistance, latency, and vaccine effectiveness.
Keywords
About the Authors
B. A. TkhorenkoRussian Federation
Boris A. Tkhorenko, Engineer and Researcher of Molecular and Cellular Biology Department
22A Voroshilova St., Kemerovo, 650056 Phone: + 7 (3842) 52-10-18
A. V. Meyer
Russian Federation
Alina V. Meyer, Associate Professor of Molecular and Cellular Biology Department
22A Voroshilova St., Kemerovo, 650056 Phone: + 7 (3842) 52-10-18
T. V. Pyanzova
Russian Federation
Tatiana V. Pyanzova, Head of Phthisiology Department
22A Voroshilova St., Kemerovo, 650056 Phone: + 7 (3842) 52-10-18
A. V. Lyamin
Russian Federation
Artem V. Lyamin, Director of Scientific and Educational Professional Center for Genetic and Laboratory Technologies
89 Chapaevskaya St., Samara, 443099 Phone: + 7 (846) 374-91-00
M. B. Lavryashina
Russian Federation
Mariya B. Lavryashina, Head of Molecular and Cellular Biology Department
22A Voroshilova St., Kemerovo, 650056 Phone: + 7 (3842) 52-10-18
References
1. Vasilyeva I.A., Testov V.V., Sterlikov S.A. Tuberculosis situation in the years of the COVID-19 pandemic – 2020-2021. Tuberculosis and Lung Diseases, 2022, vol. 100, no. 3, pp. 6-12. (In Russ.) https://doi.org/10.21292/2075-1230-2022-100-3-6-12
2. Vyazovaya A.A., Mokrousov I.V., Zhuravlev V.Yu., Solovyova N.S., Otten T.F., Manicheva O.A., Vishnevsky B.I., Narvskaya O.V. Molecular characteristics of multidrug-resistant strains of Mycobacterium tuberculosis strains in the North-West Russia. Molekulyarnaya Genetika, Mikrobiologiya i Virusologiya, 2016, vol. 34, no. 1, pp. 30-33. (In Russ.) https://doi.org/10.18821/0208-0613-2016-34-1-30-33
3. Vyazovaya A.A., Pasechnik O.A., Gerasimova A.A., Mokrousov I.V. The population structure of Beijing family of Mycobacterium tuberculosis in Western Siberia. Tuberculosis and Lung Diseases, 2020, vol. 98, no. 5, pp. 32-36. (In Russ.) https://doi.org/10.21292/2075-1230-2020-98-5-32-36
4. Moskalev A.V., Sboychakov V.B., Apchel A.V., Tsygan V.N. The modern characteristic of biology and diagnostics prospect M. tuberculosis. Bulletin of the Russian Military Medical Academy, 2018, vol. 20, no. 4, pp. 214-222. (In Russ.) https://doi.org/10.17816/brmma12368
5. Albanna A.S., Reed M.B., Kotar K.V., Fallow A., McIntosh F.A., Behr M.A., Menzies D. Reduced transmissibility of East African Indian strains of Mycobacterium tuberculosis. PLoS One, 2011, vol. 6, no. 9, pp. e25075. https://doi.org/10.1371/journal.pone.0025075
6. Barbier M., Wirth T. The Evolutionary History, Demography, and Spread of the Mycobacterium tuberculosis Complex. Microbiol. Spectr., 2016, vol. 4, no. 4. https://doi.org/10.1128/microbiolspec.TBTB2-0008-2016
7. Bespiatykh D., Bespyatykh J., Mokrousov I., Shitikov E.A. Comprehensive map of Mycobacterium tuberculosis complex regions of difference. mSphere, 2021, vol. 6, no. 4, pp. e0053521. https://doi.org/10.1128/mSphere.00535-21
8. Bespyatykh J., Shitikov E., Bespiatykh D., Guliaev A., Klimina K., Veselovsky V., Arapidi G., Dogonadze M., Zhuravlev V., Ilina E., Govorun V. Metabolic changes of Mycobacterium tuberculosis during the anti-tuberculosis therapy. Pathogens, 2020, vol. 9, no. 2, pp. 131. https://doi.org/10.3390/pathogens9020131
9. Bespyatykh J., Smolyakov A., Guliaev A., Shitikov E., Arapidi G., Butenko I., Dogonadze M., Manicheva O., Ilina E., Zgoda V., Govorun V. Proteogenomic analysis of Mycobacterium tuberculosis Beijing B0/W148 cluster strains. J. Proteomics, 2019, no. 192, pp. 18-26. https://doi.org/10.1016/j.jprot.2018.07.002
10. Blouin Y., Hauck Y., Soler C., Fabre M., Vong R., Dehan C., Cazajous G., Massoure P.L., Kraemer P., Jenkins A., Garnotel E., Pourcel C., Vergnaud G. Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One, 2012, vol. 7, no. 12, pp. e52841. https://doi.org/10.1371/journal.pone.0052841
11. Bocquet-Appel J.P. When the world's population took off: the springboard of the Neolithic Demographic Transition. Science, 2011, vol. 333, no. 6042, pp. 560-561. https://doi.org/10.1126/science.1208880
12. Bottai D., Frigui W., Sayes F., Di Luca M., Spadoni D., Pawlik A., Zoppo M., Orgeur M., Khanna V., Hardy D., Mangenot S., Barbe V., Medigue C., Ma L., Bouchier C., Tavanti A., Larrouy-Maumus G., Brosch R. TbD1 deletion as a driver of the evolutionary success of modern epidemic Mycobacterium tuberculosis lineages. Nat. Commun., 2020, vol. 11, no. 1, pp. 684. https://doi.org/10.1038/s41467-020-14508-5
13. Brites D., Gagneux S. Co-evolution of Mycobacterium tuberculosis and Homo sapiens. Immunol Rev., 2015, vol. 264, no. 1, pp. 6-24. https://doi.org/10.1111/imr.12264
14. Camus J.C., Pryor M.J., Médigue C., Cole S.T. Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. Microbiology (Reading), 2002, no. 10, pp. 2967-2973. https://doi.org/10.1099/00221287-148-10-2967
15. Chacón-Salinas R., Serafín-López J., Ramos-Payán R., Méndez-Aragón P., Hernández-Pando R., Van Soolingen D., Flores-Romo L., Estrada-Parra S., Estrada-García I. Differential pattern of cytokine expression by macrophages infected in vitro with different Mycobacterium tuberculosis genotypes. Clin. Exp. Immunol., 2005, vol. 140, no. 3, pp. 443-449. https://doi.org/10.1111/j.1365-2249.2005.02797.x
16. Cole S.T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D., Gordon S.V., Eiglmeier K., Gas S., Barry C.E. 3rd, Tekaia F., Badcock K., Basham D., Brown D., Chillingworth T., Connor R., Davies R., Devlin K., Feltwell T., Gentles S., Hamlin N., Holroyd S., Hornsby T., Jagels K., Krogh A., McLean J., Moule S., Murphy L., Oliver K., Osborne J., Quail M.A., Rajandream M.A., Rogers J., Rutter S., Seeger K., Skelton J., Squares R., Squares S., Sulston J.E., Taylor K., Whitehead S., Barrell B.G. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature, 1998, vol. 393, no. 6685, pp. 537-544. https://doi.org/10.1038/31159
17. Coll F., McNerney R., Guerra-Assunção J.A., Glynn J.R., Perdigão J., Viveiros M., Portugal I., Pain A., Martin N., Clark T.G. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat. Commun., 2014, no. 5, pp. 4812. https://doi.org/10.1038/ncomms5812
18. Conceição E.C., da Conceição M.L., Marcon D.J., Loubser J., Andrade G.L., Silva S.P.D., Cruz A.C.R., Sharma A., Suffys P., Lima K.V.B. Genomic diversity of the rarely observed genotype of the Mycobacterium tuberculosis Central Asian (CAS) lineage 3 from North Brazil. Microorganisms, 2023, vol. 11, no. 1, pp. 132. https://doi.org/10.3390/microorganisms11010132
19. Coscolla M., Gagneux S. Consequences of genomic diversity in Mycobacterium tuberculosis. Semin Immunol., 2014, vol. 26, no. 6, pp. 431- 444. https://doi.org/10.1016/j.smim.2014.09.012
20. Coscolla M., Gagneux S., Menardo F., Loiseau C., Ruiz-Rodriguez P., Borrell S., Otchere I.D., Asante-Poku A., Asare P., Sánchez-Busó L., Gehre F., Sanoussi C.N., Antonio M., Affolabi D., Fyfe J., Beckert P., Niemann S., Alabi A.S., Grobusch M.P., Kobbe R., Parkhill J., Beisel C., Fenner L., Böttger E.C., Meehan C.J., Harris S.R., de Jong B.C., Yeboah-Manu D., Brites D. Phylogenomics of Mycobacterium africanum reveals a new lineage and a complex evolutionary history. Microb. Genom., vol. 7, no. 2, pp. 000477. https://doi.org/10.1099/mgen.0.000477
21. de Jong B.C., Antonio M., Gagneux S. Mycobacterium africanum-review of an important cause of human tuberculosis in West Africa. PLoS Negl. Trop. Dis., 2010, vol. 4, no. 9, pp. e744. https://doi.org/10.1371/journal.pntd.0000744
22. Dheda K., Gumbo T., Maartens G., Dooley K.E., McNerney R., Murray M., Furin J., Nardell E.A., London L., Lessem E., Theron G., van Helden P., Niemann S., Merker M., Dowdy D., Van Rie A., Siu G.K., Pasipanodya J.G., Rodrigues C., Clark T.G., Sirgel F.A., Esmail A., Lin H.H., Atre S.R., Schaaf H.S., Chang K.C., Lange C., Nahid P., Udwadia Z.F., Horsburgh C.R. Jr., Churchyard G.J., Menzies D., Hesseling A.C., Nuermberger E., McIlleron H., Fennelly K.P., Goemaere E., Jaramillo E., Low M., Jara C.M., Padayatchi N., Warren R.M. The epidemiology, pathogenesis, transmission, diagnosis, and management of multidrug-resistant, extensively drug-resistant, and incurable tuberculosis. Lancet Respir. Med., 2017, vol. S2213-2600, no. 17, pp. 30079-30086. https://doi.org/10.1016/S2213-2600(17)30079-6
23. Dymova M.A., Kinsht V.N., Cherednichenko A.G., Khrapov E.A., Svistelnik A.V., Filipenko M.L. Highest prevalence of the Mycobacterium tuberculosis Beijing genotype isolates in patients newly diagnosed with tuberculosis in the Novosibirsk oblast, Russian Federation. J. Med. Microbiol., 2011, vol. 60, no. 7, pp. 1003-1009. https://doi.org/10.1099/jmm.0.027995-0
24. Freschi L., Vargas R. Jr., Husain A., Kamal S.M.M., Skrahina A., Tahseen S., Ismail N., Barbova A., Niemann S., Cirillo D.M., Dean A.S., Zignol M., Farhat M.R. Population structure, biogeography and transmissibility of Mycobacterium tuberculosis. Nat. Commun., 2021, vol. 12, no. 1, pp. 6099. https://doi.org/10.1038/s41467-021-26248-1
25. Gupta R.S. Phylogenomics and comparative genomic studies robustly support division of the genus mycobacterium into an emended genus mycobacterium and four novel genera. Front Microbiol., 2018, no. 9, pp. 67. https://doi.org/10.3389/fmicb.2018.00067
26. Intemann C.D., Thye T., Niemann S., Browne E.N., Amanua Chinbuah M., Enimil A., Gyapong J., Osei I., Owusu-Dabo E., Helm S., Rüsch-Gerdes S., Horstmann R.D., Meyer C.G. Autophagy gene variant IRGM -261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog., 2009, vol. 5, no. 9, pp. e1000577. https://doi.org/10.1371/journal.ppat.1000577
27. Jones R.C., Harris L.G., Morgan S., Ruddy M.C., Perry M., Williams R., Humphrey T., Temple M., Davies A.P. Phylogenetic analysis of Mycobacterium tuberculosis strains in Wales by use of core genome multilocus sequence typing to analyze whole-genome sequencing data. J. Clin Microbiol., 2019, vol. 57, no. 6, pp. e02025-18. https://doi.org/10.1128/JCM.02025-18
28. Ma R., Farrell D., Gonzalez G., Browne J.A., Nakajima C., Suzuki Y. The TbD1 Locus mediates a hypoxia-induced copper response in Mycobacterium bovis. Front Microbiol., 2022, no. 13, pp. 817952. https://doi.org/10.3389/fmicb.2022.817952
29. Mokrousov I., Shitikov E., Skiba Y., Kolchenko S., Chernyaeva E., Vyazovaya A. Emerging peak on the phylogeographic landscape of Mycobacterium tuberculosis in West Asia: Definitely smoke, likely fire Mol. Phylogenet. Evol., 2017, vol. 116, pp. 202-212. https://doi.org/10.1016/j.ympev.2017.09.002
30. Morales-Arce A.Y., Sabin S.J., Stone A.C., Jensen J.D. The population genomics of within-host Mycobacterium tuberculosis. Heredity (Edinb), 2021, vol. 126, no. 1, pp. 1-9. https://doi.org/10.1038/s41437-020-00377-7
31. Morey-León G., Andrade-Molina D., Fernández-Cadena J.C., Berná L. Comparative genomics of drug-resistant strains of Mycobacterium tuberculosis in Ecuador. BMC Genomics, 2022, vol. 23, no. 1, pp. 844. https://doi.org/10.1186/s12864-022-09042-1
32. Mutayoba B.K., Michael Hoelscher, Heinrich N., Joloba M.L., Lyamuya E., Kilale A.M., Range N.S., Ngowi B.J., Ntinginya N.E., Mfaume S.M., Wilfred A., Doulla B., Lyimo J., Kisonga R., Kingalu A., Kabahita J.M., Guido O., Kabugo J., Adam I., Luutu M.., Namaganda M.M., Namutebi J., Kasule G.W., Nakato H., Byabajungu H., Lutaaya P., Musisi K., Oola D., Mboowa G., Pletschette M. Phylogenetic lineages of tuberculosis isolates and their association with patient demographics in Tanzania. BMC Genomics, 2022, vol. 23, no. 1, pp. 561. https://doi.org/10.1186/s12864-022-08791-3
33. Netikul T., Thawornwattana Y., Mahasirimongkol S., Yanai H., Maung H.M.W., Chongsuvivatwong V., Palittapongarnpim P. Whole-genome single nucleotide variant phylogenetic analysis of Mycobacterium tuberculosis lineage 1 in endemic regions of Asia and Africa. Sci. Rep., 2022, vol. 12, no. 1, pp. 1565. https://doi.org/10.1038/s41598-022-05524-0
34. Ngabonziza J.C.S., Loiseau C., Marceau M., Jouet A., Menardo F., Tzfadia O., Antoine R., Niyigena E.B., Mulders W., Fissette K., Diels M., Gaudin C., Duthoy S., Ssengooba W., André E., Kaswa M.K., Habimana Y.M., Brites D., Affolabi D., Mazarati J.B., de Jong B.C., Rigouts L., Gagneux S., Meehan C.J., Supply P. A sister lineage of the Mycobacterium tuberculosis complex discovered in the African Great Lakes region. Nat. Commun., 2020, vol. 11, no. 1, pp. 2917. https://doi.org/10.1038/s41467-020-16626-6
35. Portevin D., Gagneux S., Comas I., Young D. Human macrophage responses to clinical isolates from the Mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog., 2011, vol. 7, no. 3, pp. e1001307. https://doi.org/10.1371/journal.ppat.1001307
36. Roetzer A., Diel R., Kohl T.A., Rückert C., Nübel U., Blom J., Wirth T., Jaenicke S., Schuback S., Rüsch-Gerdes S., Supply P., Kalinowski J., Niemann S. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLos Med., 2013, vol. 10, no. 2, pp. e1001387. https://doi.org/10.1371/journal.pmed.1001387
37. Shitikov E., Kolchenko S., Mokrousov I., Bespyatykh J., Ischenko D., Ilina E., Govorun V. Evolutionary pathway analysis and unified classification of East Asian lineage of Mycobacterium tuberculosis. Sci. Rep., 2017, vol. 7, no. 1, pp. 9227. https://doi.org/10.1038/s41598-017-10018-5
38. Shuaib Y.A., Utpatel C., Kohl T.A., Barilar I., Diricks M., Ashraf N., Wieler L.H., Kerubo G., Mesfin E.A., Diallo A.B., Al-Hajoj S., Ndung'u P., Fitzgibbon M.M., Vaziri F., Sintchenko V., Martinez E., Viegas S.O., Zhou Y., Azmy A., Al-Amry K., Godreuil S., Varma-Basil M., Narang A., Ali S., Beckert P., Dreyer V., Kabwe M., Bates M., Hoelscher M., Rachow A., Gori A.., Tekwu E.M., Sidze L.K., Jean-Paul A.A., Beng V.P., Ntoumi F., Frank M., Diallo A.G., Mboup S., Tessema B., Beyene D., Khan S.N., Diel R., Supply P., Maurer F.P., Hoffmann H., Niemann S., Merker M. Origin and global expansion of Mycobacterium tuberculosis Complex Lineage 3. Genes (Basel), 2022, vol. 13, no. 6, pp. 990. https://doi.org/10.3390/genes13060990
39. Stucki D., Brites D., Jeljeli L., Coscolla M., Liu Q., Trauner A., Fenner L., Rutaihwa L., Borrell S., Luo T., Gao Q., Kato-Maeda M., Ballif M., Egger M., Macedo R., Mardassi H., Moreno M., Tudo Vilanova G., Fyfe J., Globan M., Thomas J., Jamieson F., Guthrie J.L., Asante-Poku A., Yeboah-Manu D., Wampande E., Ssengooba W., Joloba M., Henry Boom W., Basu I., Bower J., Saraiva M., Vaconcellos S.E.G., Suffys P., Koch A., Wilkinson R., Gail-Bekker L., Malla B., Ley S.D., Beck H.P., de Jong B.C., Toit K., Sanchez-Padilla E., Bonnet M., Gil-Brusola A., Frank M., Penlap Beng V.N., Eisenach K., Alani I., Wangui Ndung'u P., Revathi G., Gehre F., Akter S., Ntoumi F., Stewart-Isherwood L., Ntinginya N.E., Rachow A., Hoelscher M., Cirillo D.M., Skenders G., Hoffner S., Bakonyte D., Stakenas P., Diel R., Crudu V., Moldovan O., Al-Hajoj S., Otero L., Barletta F., Jane Carter E., Diero L., Supply P., Comas I, Niemann S, Gagneux S. Mycobacterium tuberculosis lineage 4 comprises globally distributed and geographically restricted sublineages. Nat. Genet., 2016, 48, no. 12, pp. 1535-1543. https://doi.org/10.1038/ng.3704
40. Thawornwattana Y., Mahasirimongkol S., Yanai H., Maung H.M.W., Cui Z., Chongsuvivatwong V., Palittapongarnpim P. Revised nomenclature and SNP barcode for Mycobacterium tuberculosis lineage 2. Microb. Genom., 2021, vol. 7, no. 11, pp. 000697. https://doi.org/10.1099/mgen.0.000697
41. Traore B., Diarra B., Dembele B.P., Somboro A.M., Hammond A.S., Siddiqui S., Maiga M., Kone B., Sarro Y.S., Washington J., Parta M., Coulibaly N., M'baye O., Diallo S., Koita O., Tounkara A., Polis M.A. Molecular strain typing of Mycobacterium tuberculosis complex in Bamako, Mali. Int. J. Tuberc. Lung Dis., 2012, vol. 16, no. 7, pp. 911-916. https://doi.org/10.5588/ijtld.11.0397
42. van Ingen J., Rahim Z., Mulder A., Boeree M.J., Simeone R., Brosch R., van Soolingen D. Characterization of Mycobacterium orygis as M. tuberculosis complex subspecies. Emerging Infectious Diseases, 2012, vol. 18, no. 4, pp. 653– 655. https://doi.org/10.3201/eid1804.110888
43. Vasconcellos S.E., Huard R.C., Niemann S., Kremer K., Santos A.R., Suffys P.N., Ho J.L. Distinct genotypic profiles of the two major clades of Mycobacterium africanum. BMC Infectious Diseases, 2010, no. 10, pp. 80. https://doi.org/10.1186/1471-2334-10-80
44. Yimer S.A., Namouchi A., Zegeye E.D., Holm-Hansen C., Norheim G., Abebe M., Aseffa A., Tønjum T. Deciphering the recent phylogenetic expansion of the originally deeply rooted Mycobacterium tuberculosis lineage 7. BMC Evol. Biol., 2016, vol. 16, no. 1, pp. 146. https://doi.org/10.1186/s12862-016-0715-z
Review
For citations:
Tkhorenko B.A., Meyer A.V., Pyanzova T.V., Lyamin A.V., Lavryashina M.B. Insights into Population Genetics and Phylogeography of Mycobacterium tuberculosis. Tuberculosis and Lung Diseases. 2024;102(5):91-98. (In Russ.) https://doi.org/10.58838/2075-1230-2024-102-5-91-98