Abstract
Mycobacterium avium subsp. hominissuis (MAH) are typical inhabitants of the environment, which are known as opportunistic pathogens of animals and humans. The aim of our study was to analyze single-nucleotide polymorphisms (SNPs) in the hsp65 and MACPPE12 genes to characterize the Russian population of MAH in the context of studying phylogenetic relationships and the evolution of geographically distant populations of M. avium subsp. hominissuis. The sequence analysis of the hsp65 and MACPPE12 genes was applied for 40 MAH strains isolated from humans (patients with mycobacteriosis). The nucleotide sequences were aligned to the reference genome of M. avium subsp. hominissuis 104 (accession no. NC_008595.1). The mutational profiles of Russian strains were compared with those isolated in other countries. In total, 40 MAH strains were classified into three different hsp65 sequevars: code 1, code 2, and code 3. The majority of MAH strains (72.5%) belonged to code 1, the same sequevar as for MAH strain 104. The sequence analysis of the MACPPE12 gene revealed 20 SNPs grouped into nine sequevars at the nucleic acid level: NA01, NA02, NA03, NA06, NA10, NA13, NA14, NA19, and NA_Rus01. Eight out of 20 SNPs were nonsynonymous, resulting in seven sequevars at the amino acid level: AA01, AA02, AA04, AA07, AA08, AA13, and AA_Rus01. The sequevar AA02 consisted of three different NA variants with synonymous SNPs profiles: NA02, NA03, and NA06. Half of the MAH strains belonged to the sequevar AA02 (type NA02). The predominant cluster AA02 (type NA02)/code 1 and the unique variant AA_Rus01 (NA_Rus01) were identified among MAH strains from Russia. Thus, we confirmed the relative conservativeness of the nucleotide sequence of the hsp65 gene but the polymorphism of the MACPPE12 gene. At the same time, a comparative analysis of the SNPs profiles of the hsp65 and MACPPE12 genes allowed us to identify differences and similarities between geographically distant populations of MAH, which highlighted the variability of the global population of M. avium species.
Similar content being viewed by others
REFERENCES
Otten, T.F. and Vasil’ev, A.V., Mikobakterioz (Mycobacteriosis), St. Petersburg: Meditsinskaya Pressa, 2005.
Levy-Frebault, V.V. and Portaels, F., Proposed minimal standards for the genus Mycobacterium and for description of new slowly growing Mycobacterium species, Int. J. Syst. Bacteriol., 1992, vol. 42, pp. 315—323.
Shinnick, T.M. and Good, R.C., Mycobacterial taxonomy, Eur. J. Clin. Mycrobiol. Infect. Dis., 1994, vol. 13, no. 11, pp. 884—901.
Iwamoto, T., Nakajima, C., Nishiuchi, Y., et al., Genetic diversity of Mycobacterium avium subsp. hominissuis strains isolated from humans, pigs, and human living environment, Infect. Genet. Evol., 2012, vol. 12, no. 4, pp. 846—852.
Falkinham, III J.O., Nontuberculous mycobacteria in the environment, Clin. Chest Med., 2002, vol. 23, no. 3, pp. 529—551.
Turenne, C.Y., Wallace, R., and Behr, M.A., Mycobacterium avium in the postgenomic era, Clin. Microb. Rev., 2007, vol. 20, no. 2, pp. 205—229.
Rindi, L. and Garzelli, C., Genetic diversity and phylogeny of Mycobacterium avium, Infect. Genet. Evol., 2014, vol. 21, no. 4, pp. 375—383.
Chimara, E., Ferrazoli, L., Ueky, S.Y.M., et al., Reliable identification of mycobacterial species by PCR-restriction enzyme analysis (PRA)-hsp65 in a reference laboratory and elaboration of a sequence-based extended algorithm of PRA-hsp65 patterns, BMC Microbiol., 2008, vol. 8, no. 48. https://doi.org/10.1186/1471-2180-8-48
McNabb, A., Eisler, D., Adie, K., et al., Assessment of partial sequencing of the 65-kilodalton heat shock protein gene (hsp65) for routine identification of Mycobacterium species isolated from clinical sources, J. Clin. Microbiol., 2004, vol. 42, no. 7, pp. 3000—3011.
Telenti, A., Marchesi, F., Balz, M., et al., Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis, J. Clin. Microbiol., 1993, vol. 31, no. 2, pp. 175—178.
Sampson, S.L., Mycobacterial PE/PPE proteins at the host—pathogen interface, Clin. Dev. Immunol., 2011. https://doi.org/10.1155/2011/497203
Mackenzie, N., Alexander, D.C., Turenne, C.Y., et al., Genomic comparison of PE and PPE genes in the Mycobacterium avium complex, J. Clin. Microbiol., 2009, vol. 47, pp. 1002—1011.
Iwamoto, T., Arikawa, K., Nakajima, C., et al., Intra-subspecies sequence variability of the MACPPE12 gene in Mycobacterium avium subsp. hominissuis, Genet. Evol., 2014, vol. 21, pp. 479—483.
Starkova, D.A., Otten, T.F., Mokrousov, I.V., et al., Genotypic characteristics of Mycobacterium avium subsp. hominissuis strains, Russ. J. Genet., 2013, vol. 49, no. 9, pp. 909—914. https://doi.org/10.1134/S1022795413090093
Starkova, D.A., Mokrousov, I.V., Vyazovaya, A.A., et al., Genome polymorphism of Mycobacterium avium subsp. hominissuis strains, Mol. Genet., Microbiol. Virol., 2014, vol. 29, no. 4, pp. 172—178.
Van Embden, J.D., Cave, M.D., Crawford, J.T., et al., Strain identification on Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology, J. Clin. Microbiol., 1993, vol. 31, no. 2, pp. 406—409.
Bartos, M., Hlozek, P., Svastova, P., et al., Identification of members of Mycobacterium avium species by Accu-Probes, serotyping, and single IS900, IS901, IS1245 and IS901-flanking region PCR with internal standards, J. Microbiol. Methods, 2006, vol. 64, no. 3, pp. 333—345.
Inagaki, T., Nishimori, K., Yagi, T., et al., Comparison of a Variable-Number Tandem-Repeat (VNTR) method for typing Mycobacterium avium with Mycobacterial Interspersed Repetitive-Unit—VNTR and IS1245 restriction fragment length polymorphism typing, J. Clin. Microbiol., 2009, vol. 47, no. 7, pp. 2156—2164.
Thibault, V.C., Grayon, M., Boschiroli, M., et al., New Variable-Number Tandem-Repeat markers for typing Mycobacterium avium subsp. paratuberculosis and M. avium strains: comparison with IS900 and IS1245 restriction fragment length polymorphism typing, J. Clin. Microbiol., 2007, vol. 45, no. 8, pp. 2404—2410.
Turenne, C.Y., Semret, M., Cousins, D.V., et al., Sequencing of hsp65 distinguishes among subsets of the Mycobacterium avium complex, J. Clin. Microbiol., 2006, vol. 44, no. 2, pp. 433—440. https://doi.org/10.1128/JCM.44.2.433-440.2006
Kim, S.-Y., Jeong, B.-H., Park, H.Y., et al., Association of ISMav6 with the pattern of antibiotic resistance in Korean Mycobacterium avium clinical isolates but no relevance between their genotypes and clinical features, PLoS One, 2016, vol. 11, no. 2. https://doi.org/10.1371/journal.pone.0148917
Scherrer, S., Landolt, P., Carroli, N., and Stephan, R., Molecular characterization of Mycobacterium avium subsp. hominissuis of two groups of lymph nodes, being intradermal tuberculin or interferon-gamma test positive and negative, isolated from Swiss cattle at slaughter, Front. Vet. Sci., 2018, vol. 5, no. 32. https://doi.org/10.3389/fvets.2018.00032
Vluggen, C., Soetaert, K., Duytschaever, L., et al., Genotyping and strain distribution of Mycobacterium avium subspecies hominissuis isolated from humans and pigs in Belgium, 2011—2013, Euro Surveill., 2016, vol. 21, no. 3. http://dx.doi.org/10.2807/1560 7917.ES.2016.21.3.30111.
Author information
Authors and Affiliations
Corresponding author
Additional information
Devoted to the memory of Tatiana Ferdinandovna Otten, Dr. Sci. (Biology), TB specialist
Translated by E. Makeeva
Rights and permissions
About this article
Cite this article
Starkova, D.A., Iwamoto, T., Vyazovaya, A.A. et al. Single Nucleotide Polymorphisms in hsp65 and MACPPE12 Genes of Mycobacterium avium subsp. hominissuis. Russ J Genet 55, 544–550 (2019). https://doi.org/10.1134/S1022795419050120
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1022795419050120