Blood and sputum microbiota composition in Afghan immigrants and Iranian subjects with pulmonary tuberculosis
-
Ali Nour Neamatollahi
,
Samira Tarashi
,
Nayereh Ebrahimzadeh
,
Farzam Vaziri
,
Mohammad Ali Zaheri Birgani
,
Mohammadreza Aghasadeghi
,
Abolfazl Fateh
,
Seyed Davar Siadat
,
Saeid Bouzari
Abstract
Background and Objectives: TB infection is one of the most challengeable epidemiological issues. Complex interactions between microbiota and TB infection have been demonstrated. Alteration in microbial population during TB infection may act as a useful biomarker. The present study examined the microbiota patterns of blood and sputum samples collected from Afghan immigrants and Iranian patients with active TB.
Materials and Methods: Sixty active pulmonary TB patients were enrolled in the study. Blood and sputum samples were collected. To detect phylum bacterial composition in the blood and sputum samples, bacterial 16S rRNA quantification by Real-Time qPCR was performed.
Results: A significant decrease in Bacteroidetes in Iranian sputum and blood samples of Afghan immigrants and Iranian TB active subjects were seen. While, sputum samples of Afghan immigrants showed no significant differences in Bacteroidetes abundance among TB active and control. Firmicutes were also presented no significant difference between sputum samples of the two races. Actinobacteria showed a significant increase in Iranian and Afghan sputum samples while this phylum showed no significant abundance in Iranian and Afghan TB positive blood samples. Proteobacteria also showed an increase in sputum and blood samples of the two races.
Conclusion: An imbalance in Bacteroidetes and Firmicutes abundance may cause an alteration in the microbiota composition, resulting in dysregulated immune responses and resulting in the augmentation of opportunistic pathogens during TB infection, notably Proteobacteria and Actinobacteria. Evaluation of human microbiota under different conditions of TB infection can be critical to a deeper understanding of the disease control.
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28. Sharma R, Saikia UN, Sharma S, Verma I. Activity of human beta defensin-1 and its motif against active and dormant Mycobacterium tuberculosis. Appl Microbiol Biotechnol 2017; 101: 7239-7248.
29. Stark JM, Tibbitt CA, Coquet JM. The metabolic requirements of Th2 cell differentiation. Front Immunol 2019; 10: 2318.
30. Nastasi C, Fredholm S, Willerslev-Olsen A, Hansen M, Bonefeld CM, Geisler C, et al. Butyrate and propionate inhibit antigen-specific CD8+ T cell activation by suppressing IL-12 production by antigen-presenting cells. Sci Rep 2017; 7: 14516.
31. Piccinni M-P, Lombardelli L, Logiodice F, Kullolli O, Maggi E, Barkley MS. Medroxyprogesterone acetate decreases Th1, Th17, and increases Th22 responses via AHR signaling which could affect susceptibility to infections and inflammatory disease. Front Immunol 2019; 10: 642.
32. Zafar H, Saier MH Jr. Gut Bacteroides species in health and disease. Gut Microbes 2021; 13: 1-20.
33. Stojanov S, Berlec A, Štrukelj B. The influence of probiotics on the firmicutes/bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms 2020; 8: 1715.
34. Perveen S, Sharma R. Lung Microbiome: Friend or Foe of Mycobacterium tuberculosis. Microbiome in Inflammatory Lung Diseases: Springer; 2022. p. 207-226.
35. Huang Y, Tang J-H, Cai Z, Qi Y, Jiang S, Ma T-T, et al. Alterations in the nasopharyngeal microbiota associated with active and latent tuberculosis. Tuberculosis (Edinb) 2022; 136: 102231.
36. Pujic P, Beaman BL, Ravalison M, Boiron P, Rodríguez-Nava V. Nocardia and Actinomyces. Mol Med Microbiol: Elsevier; 2015. p. 731-752.
37. Kanangat S, Skaljic I. Microbiome analysis, the immune response and transplantation in the era of next generation sequencing. Hum Immunol 2021; 82: 883-901.
2. World Health Organization (2020). Global tuberculosis report. https://www.who.int/publications/i/item/9789240013131
3. McQuaid CF, Vassall A, Cohen T, Fiekert K, White RG. The impact of COVID-19 on TB: a review of the data. Int J Tuberc Lung Dis 2021; 25: 436-446.
4. Trajman A, Felker I, Alves LC, Coutinho I, Osman M, Meehan S-A, et al. The COVID-19 and TB syndemic: the way forward. Int J Tuberc Lung Dis 2022; 26: 710-719.
5. Bialvaei AZ, Asgharzadeh M, Aghazadeh M, Nourazarian M, Kafil HS. Challenges of tuberculosis in Iran. Jundishapur J Microbiol 2017; 10(3): e37866.
6. Tarashi S, Badi SA, Moshiri A, Ebrahimzadeh N, Fateh A, Vaziri F, et al. The inter-talk between Mycobacterium tuberculosis and the epigenetic mechanisms. Epigenomics 2020; 12: 455-469.
7. Wang J, Xiong K, Zhao S, Zhang C, Zhang J, Xu L, et al. Long-term effects of multi-drug-resistant tuberculosis treatment on gut microbiota and its health consequences. Front Microbiol 2020; 11: 53.
8. Huang HL, Luo YC, Lu PL, Huang CH, Lin KD, Lee MR, et al. Gut microbiota composition can reflect immune responses of latent tuberculosis infection in patients with poorly controlled diabetes. Respir Res 2023; 24: 11.
9. Castillo DJ, Rifkin RF, Cowan DA, Potgieter M. The healthy human blood microbiome: fact or fiction? Front Cell Infect Microbiol 2019; 9: 148.
10. Tarashi S, Ahmadi Badi S, Moshiri A, Nasehi M, Fateh A, Vaziri F, et al. The human microbiota in pulmonary tuberculosis: Not so innocent bystanders. Tuberculosis (Edinb) 2018; 113: 215-221.
11. Hang J, Desai V, Zavaljevski N, Yang Y, Lin X, Satya RV, et al. 16S rRNA gene pyrosequencing of reference and clinical samples and investigation of the temperature stability of microbiome profiles. Microbiome 2014; 2: 31.
12. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73: 5261-5267.
13. Bengtsson‐Palme J, Hartmann M, Eriksson KM, Pal C, Thorell K, Larsson DG, et al. METAXA2: improved identification and taxonomic classification of small and large subunit rRNA in metagenomic data. Mol Ecol Resour 2015; 15: 1403-1414.
14. Peterson J, Garges S, Giovanni M, McInnes P, Wang L, Schloss JA, et al. The NIH human microbiome project. Genome Res 2009; 19: 2317-2323.
15. Dang AT, Marsland BJ. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol 2019; 12: 843-850.
16. Zhang D, Li S, Wang N, Tan H-Y, Zhang Z, Feng Y. The cross-talk between gut microbiota and lungs in common lung diseases. Front Microbiol 2020; 11: 301.
17. Vacca I. Microbiota: Clostridia protect from gut infections in early life. Nat Rev Microbiol 2017; 15: 321.
18. Serino M. Molecular paths linking metabolic diseases, gut microbiota dysbiosis and enterobacteria infections. J Mol Biol 2018; 430: 581-590.
19. Wipperman MF, Bhattarai SK, Vorkas CK, Maringati VS, Taur Y, Mathurin L, et al. Gastrointestinal microbiota composition predicts peripheral inflammatory state during treatment of human tuberculosis. Nat Commun 2021; 12: 1141.
20. Osei Sekyere J, Maningi NE, Fourie PB. Mycobacterium tuberculosis, antimicrobials, immunity, and lung–gut microbiota crosstalk: Current updates and emerging advances. Ann N Y Acad Sci 2020; 1467: 21-47.
21. Pei J, Yang Y, Zhou X, Hu G, Wang X, Guo Y, et al. Relationship between tuberculosis and microbiota. Chin J Appl Clin Pediatr 2020; (24): 775-779.
22. Sánchez-Tapia M, Tovar AR, Torres N. Diet as regulator of gut microbiota and its role in health and disease. Arch Med Res 2019; 50: 259-268.
23. Feng W, Ao H, Peng C. Gut microbiota, short-chain fatty acids, and herbal medicines. Front Pharmacol 2018; 9: 1354.
24. Cheung MK, Lam WY, Fung WY, Law PT, Au CH, Nong W, et al. Sputum microbiota in tuberculosis as revealed by 16S rRNA pyrosequencing. PLoS One 2013; 8(1): e54574.
25. Del Carpio-Sanz AO, Revilla-Mogrovejo CR, Luna-Paredes LF, Ttito-Velasquez K, Cáceres-Zegarra RA, Chávez-Arias TS, et al. Identification of the microbiome present in sputum samples from patients with clinical tuberculosis by NGS (Next generation sequencing). Nat Volatiles Essent Oils 2021; 8: 4198-4217.
26. Shah T, Shah Z, Baloch Z, Cui X. The role of microbiota in respiratory health and diseases, particularly in tuberculosis. Biomed Pharmacother 2021; 143: 112108.
27. Fachi JL, Sécca C, Rodrigues PB, Mato FCP, Di Luccia B, Felipe JS, et al. Acetate coordinates neutrophil and ILC3 responses against C. difficile through FFAR2. J Exp Med 2020; 217: jem.20190489.
28. Sharma R, Saikia UN, Sharma S, Verma I. Activity of human beta defensin-1 and its motif against active and dormant Mycobacterium tuberculosis. Appl Microbiol Biotechnol 2017; 101: 7239-7248.
29. Stark JM, Tibbitt CA, Coquet JM. The metabolic requirements of Th2 cell differentiation. Front Immunol 2019; 10: 2318.
30. Nastasi C, Fredholm S, Willerslev-Olsen A, Hansen M, Bonefeld CM, Geisler C, et al. Butyrate and propionate inhibit antigen-specific CD8+ T cell activation by suppressing IL-12 production by antigen-presenting cells. Sci Rep 2017; 7: 14516.
31. Piccinni M-P, Lombardelli L, Logiodice F, Kullolli O, Maggi E, Barkley MS. Medroxyprogesterone acetate decreases Th1, Th17, and increases Th22 responses via AHR signaling which could affect susceptibility to infections and inflammatory disease. Front Immunol 2019; 10: 642.
32. Zafar H, Saier MH Jr. Gut Bacteroides species in health and disease. Gut Microbes 2021; 13: 1-20.
33. Stojanov S, Berlec A, Štrukelj B. The influence of probiotics on the firmicutes/bacteroidetes ratio in the treatment of obesity and inflammatory bowel disease. Microorganisms 2020; 8: 1715.
34. Perveen S, Sharma R. Lung Microbiome: Friend or Foe of Mycobacterium tuberculosis. Microbiome in Inflammatory Lung Diseases: Springer; 2022. p. 207-226.
35. Huang Y, Tang J-H, Cai Z, Qi Y, Jiang S, Ma T-T, et al. Alterations in the nasopharyngeal microbiota associated with active and latent tuberculosis. Tuberculosis (Edinb) 2022; 136: 102231.
36. Pujic P, Beaman BL, Ravalison M, Boiron P, Rodríguez-Nava V. Nocardia and Actinomyces. Mol Med Microbiol: Elsevier; 2015. p. 731-752.
37. Kanangat S, Skaljic I. Microbiome analysis, the immune response and transplantation in the era of next generation sequencing. Hum Immunol 2021; 82: 883-901.
| Files | ||
| Issue | Vol 16 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i3.15766 | |
| Keywords | ||
| Mycobacterium tuberculosis; Bacteroidetes; Firmicutes; Actinobacteria; Proteobacteria | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Nour Neamatollahi A, Tarashi S, Ebrahimzadeh N, Vaziri F, Zaheri Birgani MA, Aghasadeghi M, Fateh A, Siadat SD, Bouzari S. Blood and sputum microbiota composition in Afghan immigrants and Iranian subjects with pulmonary tuberculosis. Iran J Microbiol. 2024;16(3):342-350.
