Skip to main content

Microbiome diversity in the sputum of patients with pulmonary tuberculosis

European Journal of Clinical Microbiology & Infectious Diseases volume 35, pages 1205–1210 (2016)Cite this article

Abstract

TB is a worldwide pandemic. India has the highest burden of TB, with WHO statistics for 2013 giving an estimated incidence figure of 2.1 million cases for India out of a global incidence of 9 million. Microbiota have been shown to be associated with many disease conditions; however, only few studies have been reported for microbiota associated with TB infection. For the first time, we characterized the composition of microbiota of TB patients of India, using high-throughput 16S rRNA gene sequencing and compared it with healthy controls. Phylum-level analysis showed that the relative abundance of Firmicutes and Actinobacteria was significantly higher in TB samples and Neisseria and Veillonella were two dominant genera after Streptococcus. In our study, significantly different core genera in TB and normal population were found as compared with the reported studies. Also, the presence of diverse opportunistic pathogenic microbiota in TB patients increases the complexity and diversity of sputum microbiota. Characterization of the sputum microbiome is likely to provide important pathogenic insights into pulmonary tuberculosis.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig 1
Fig 2
Fig 3

References

  1. WHO (2014) Global tuberculosis report 2014. World Health Organuisation, Geneva

    Google Scholar 

  2. Zhou Y, Lin P, Li Q, Han L, Zheng H, Wei Y, Cui Z, Ni Y, Guo X (2010) Analysis of the microbiota of sputum samples from patients with lower respiratory tract infections. Acta Biochim Biophys Sin Shanghai 42(10):754–761

    Article  PubMed  Google Scholar 

  3. Pedron T, Sansonetti P (2008) Commensals bacterial pathogens and intestinal inflammation: an intriguing menage a trois. Cell Host Microbe 3:344–347

    CAS  Article  PubMed  Google Scholar 

  4. Bisen PS (2015) Potential of microbiome research in respiratory diseases. J Respir Res 1(1):13–14

    Google Scholar 

  5. Zacharia AJ, Jain A, Raghuvanshi R, Kumar A, Prasad GBKS, Bisen PS (2016) Gas chromatography and mass spectroscopy based detection of autoinducer-2 like molecule in the circulation of tuberculosis infected cases. J Respir Res 2(1):33–36

    Google Scholar 

  6. Blaser MJ, Falkow S (2009) What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 7(12):887–894

    CAS  Article  PubMed  Google Scholar 

  7. Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI et al (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. The Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214

    Article  PubMed Central  Google Scholar 

  9. Ling Z, Kong J, Liu F, Zhu H, Chen X et al (2010) Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11:488

    Article  PubMed  PubMed Central  Google Scholar 

  10. Charlson ES, Bittinger K, Chen J, Diamond JM, Li H et al (2012) Assessing bacterial populations in the lung by replicate analysis of samples from the upper and lower respiratory tracts. Plos One 7, e42786

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Lazarevic V, Whiteson K, Huse S, Hernandez D, Farinelli L et al (2009) Metagenomic study of the oral microbiota by Illumina high-throughput sequencing. J Microbiol Methods 79:266–271

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Erb-Downward JR, Thompson DL, Han MK, Freeman CM, McCloskey L et al (2011) Analysis of the lung microbiome in the “healthy” smoker and in COPD. Plos One 6, e16384

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Cui Z, Zhou Y, Li H, Zhang Y, Zhang S et al (2012) Complex sputum microbial composition in patients with pulmonary tuberculosis. BMC Microbiol 12:276

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Cheung MK, Lam WY, Fung WY, Law PT, Au CH et al (2013) Sputum microbiota in tuberculosis as revealed by 16S rRNA pyrosequencing. Plos One 8, e54574

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Wu J, Liu W, He L, Huang F, Chen J, Cui P et al (2013) Sputum microbiota associated with new, recurrent and treatment failure tuberculosis. Plos One 8(12), e83445

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bhat J, Rao VG, Yadav R, Muniyandi M, Sharma R, Karfarma C, Luke C (2015) Situation of drug resistant tuberculosis in Saharia tribe of central India. Indian J Med Res 141(5):636–639

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cabrera-Rubio R, Garcia-Núñez M, Setó L, Antó JM, Moya A et al (2012) Microbiome diversity in the bronchial tract of patients with chronic obstructive pulmonary disease. J Clin Microbiol 50:3562–3568

    Article  PubMed  PubMed Central  Google Scholar 

  18. Coburn B, Wang PW, Diaz Caballero J, Clark ST, Brahma V et al (2015) Lung microbiota across age and disease stage in cystic fibrosis. Sci Rep 5:10241

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Fusconi M, Conti C, de Virgilio A, Vincentiis M (2009) Polmonite paucisintomatica da Rothia mucilaginosa: caso clinica e rassegna della letteratura. Infez Med 2:100–104

    Google Scholar 

  20. Baeza Martínez C, Zamora Molina L, García Sevila R, Gil Carbonell J, Ramos Rincon JM, Martín Serrano C (2014) Rothia mucilaginosa pneumonia in an immunocompetent patient. Arch Bronconeumol 50(11):493–495

    Article  PubMed  Google Scholar 

  21. Loughrey AC, Chew EW (1990) Endocarditis caused by Veillonella dispar. J Infect 21:319–321

    CAS  Article  PubMed  Google Scholar 

  22. Houston SD, Taylor D, Rennie R (1997) Prosthetic valve endocarditis due to Veillonella dispar: successful medical treatment following penicillin desensitization. Clin Infect Dis 24:1013–1014

    CAS  Article  PubMed  Google Scholar 

  23. Fisher K, Phillips C (2009) The ecology, epidemiology and virulence of Enterococcus. Microbiology 155:1749–1757

    CAS  Article  PubMed  Google Scholar 

  24. Parameswaran G, Wrona CT, Murphy TF, Sethi S (2009) Moraxella catarrhalis acquisition, airway inflammation and protease-antiprotease balance in chronic obstructive pulmonary disease. BMC Infect Dis 9:178

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Grand Challenges Canada (ID S4 0253-01) for providing financial assistance to support this study, to Dr. Anish Zacharia J, Sun Pharmaceutical Industries Limited, India for collection of samples from Gajra Raja Medical College, Gwalior, India, and to Devashish Ohri, Executive Vice President-APAC and Shyam Sharma, Vice President-Diagnostics APAC, Avantor Performance Materials India Limited for their support and providing infrastructure. Bioinformatics support was provided by 1st BASE Laboratories, Singapore.

Author information

Author notes

    Affiliations

    1. Diagnostics R&D, Avantor Performance Materials India Limited (formerly RFCL Limited), New Delhi, 110020, India

      P. Krishna & A. Jain

    2. School of Studies in Biotechnology, Jiwaji University, Gwalior, 474011 M.P., India

      P. S. Bisen

    Authors
    1. P. Krishna
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. A. Jain
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. P. S. Bisen
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to P. S. Bisen.

    Ethics declarations

    Funding

    Grand Challenges Canada, Grant ID S4 0253-01.

    Conflict of interest

    The authors declare that there is no conflict of interest.

    Ethical approval

    All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

    Informed consent

    Written consent was obtained from all the studied patients for sample collection and subsequent analysis.

    Additional information

    Pankaj Krishna and Anubhav Jain contributed equally as first author.

    Rights and permissions

    Reprints and Permissions

    About this article

    Verify currency and authenticity via CrossMark

    Cite this article

    Krishna, P., Jain, A. & Bisen, P.S. Microbiome diversity in the sputum of patients with pulmonary tuberculosis. Eur J Clin Microbiol Infect Dis 35, 1205–1210 (2016). https://doi.org/10.1007/s10096-016-2654-4

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10096-016-2654-4

    Keywords

    • Normal Sample
    • Pulmonary Tuberculosis
    • Lower Respiratory Tract Infection
    • Core Genus
    • Sputum Sample