Pathogenic Determinants of the Mycobacterium kansasii Complex: An Unsuspected Role for Distributive Conjugal Transfer
Abstract
1. Introduction
2. Materials and Methods
2.1. Strain Inclusion and Pathogenicity Classification
2.2. Bacterial Cultures, DNA Extraction and Sequencing
2.3. Quality Controls, Assembly, Annotation and Comparative Genomic Analyses
2.4. Detection of Distributive Conjugal Transfers between Members of the M. kansasii Complex
2.5. Detection of Conjugative Plasmids
3. Results
3.1. M. kansasii Is More Pathogenic than Other Members of the Complex
3.2. Genomic Features and Core-Genome Phylogeny
3.3. Virulence Factors of the M. kansasii Complex
3.4. Three Distributive Conjugal Transfers Induced Gene Losses Associated with Pathogenicity
3.5. Conjugative Plasmids Are Widespread but Not Associated with Pathogenicity
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Field, S.K.; Cowie, R.L. Lung Disease Due to the More Common Nontuberculous Mycobacteria. Chest 2006, 129, 1653–1672. [Google Scholar] [CrossRef]
- Prevots, D.R.; Marras, T.K. Epidemiology of Human Pulmonary Infection with Nontuberculous Mycobacteria: A Review. Clin. Chest Med. 2015, 36, 13–34. [Google Scholar] [CrossRef]
- Griffith, D.E.; Aksamit, T.; Brown-Elliott, B.A.; Catanzaro, A.; Daley, C.; Gordin, F.; Holland, S.M.; Horsburgh, R.; Huitt, G.; Iademarco, M.F.; et al. An Official ATS/IDSA Statement: Diagnosis, Treatment, and Prevention of Nontuberculous Mycobacterial Diseases. Am. J. Respir. Crit. Care Med. 2007, 175, 367–416. [Google Scholar] [CrossRef]
- Bhatt, K.; Banavathi, K. Mycobacterium Kansasii Osteomyelitis—A Masquerading Disease. JMM Case Rep. 2018, 5, e005114. [Google Scholar] [CrossRef]
- Alvarado-Esquivel, C.; García-Corral, N.; Carrero-Dominguez, D.; Enciso-Moreno, J.A.; Gurrola-Morales, T.; Portillo-Gómez, L.; Rossau, R.; Mijs, W. Molecular Analysis of Mycobacterium Isolates from Extrapulmonary Specimens Obtained from Patients in Mexico. BMC Clin. Pathol. 2009, 9, 1. [Google Scholar] [CrossRef]
- Brooker, W.J.; Aufderheide, A.C. Genitourinary Tract Infections Due to Atypical Mycobacteria. J. Urol. 1980, 124, 242–244. [Google Scholar] [CrossRef]
- Alcaide, F.; Richter, I.; Bernasconi, C.; Springer, B.; Hagenau, C.; Schulze-Röbbecke, R.; Tortoli, E.; Martín, R.; Böttger, E.C.; Telenti, A. Heterogeneity and Clonality among Isolates of Mycobacterium Kansasii: Implications for Epidemiological and Pathogenicity Studies. J. Clin. Microbiol. 1997, 35, 1959–1964. [Google Scholar] [CrossRef]
- Devallois, A.; Goh, K.S.; Rastogi, N. Rapid Identification of Mycobacteria to Species Level by PCR-Restriction Fragment Length Polymorphism Analysis of the Hsp65 Gene and Proposition of an Algorithm to Differentiate 34 Mycobacterial Species. J. Clin. Microbiol. 1997, 35, 2969–2973. [Google Scholar] [CrossRef]
- Bakuła, Z.; Modrzejewska, M.; Safianowska, A.; van Ingen, J.; Proboszcz, M.; Bielecki, J.; Jagielski, T. Proposal of a New Method for Subtyping of Mycobacterium Kansasii Based upon PCR Restriction Enzyme Analysis of the Tuf Gene. Diagn. Microbiol. Infect. Dis. 2016, 84, 318–321. [Google Scholar] [CrossRef]
- Tagini, F.; Aeby, S.; Bertelli, C.; Droz, S.; Casanova, C.; Prod’hom, G.; Jaton, K.; Greub, G. Phylogenomics Reveal That Mycobacterium Kansasii Subtypes Are Species-Level Lineages. Description of Mycobacterium Pseudokansasii Sp. Nov., Mycobacterium Innocens Sp. Nov. and Mycobacterium Attenuatum Sp. Nov. Int. J. Syst. Evol. Microbiol. 2019, 69, 1696–1704. [Google Scholar] [CrossRef]
- Taillard, C.; Greub, G.; Weber, R.; Pfyffer, G.E.; Bodmer, T.; Zimmerli, S.; Frei, R.; Bassetti, S.; Rohner, P.; Piffaretti, J.-C.; et al. Clinical Implications of Mycobacterium Kansasii Species Heterogeneity: Swiss National Survey. J. Clin. Microbiol. 2003, 41, 1240–1244. [Google Scholar] [CrossRef]
- Shahraki, A.H.; Trovato, A.; Mirsaeidi, M.; Borroni, E.; Heidarieh, P.; Hashemzadeh, M.; Shahbazi, N.; Cirillo, D.M.; Tortoli, E. Mycobacterium Persicum Sp. Nov., a Novel Species Closely Related to Mycobacterium Kansasii and Mycobacterium Gastri. Int. J. Syst. Evol. Microbiol. 2017, 67, 1766–1770. [Google Scholar] [CrossRef] [PubMed]
- Jagielski, T.; Borówka, P.; Bakuła, Z.; Lach, J.; Marciniak, B.; Brzostek, A.; Dziadek, J.; Dziurzyński, M.; Pennings, L.; van Ingen, J.; et al. Genomic Insights Into the Mycobacterium Kansasii Complex: An Update. Front. Microbiol. 2020, 10, 2918. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; McIntosh, F.; Radomski, N.; Dewar, K.; Simeone, R.; Enninga, J.; Brosch, R.; Rocha, E.P.; Veyrier, F.J.; Behr, M.A. Insights on the Emergence of Mycobacterium Tuberculosis from the Analysis of Mycobacterium Kansasii. Genome Biol. Evol. 2015, 7, 856–870. [Google Scholar] [CrossRef]
- Gröschel, M.I.; Sayes, F.; Simeone, R.; Majlessi, L.; Brosch, R. ESX Secretion Systems: Mycobacterial Evolution to Counter Host Immunity. Nat. Rev. Microbiol. 2016, 14, 677–691. [Google Scholar] [CrossRef]
- Ma, Y.; Keil, V.; Sun, J. Characterization of Mycobacterium Tuberculosis EsxA Membrane Insertion: Roles of N- and C-Terminal Flexible Arms and Central Helix-Turn-Helix Motif. J. Biol. Chem. 2015, 290, 7314–7322. [Google Scholar] [CrossRef]
- Simeone, R.; Bobard, A.; Lippmann, J.; Bitter, W.; Majlessi, L.; Brosch, R.; Enninga, J. Phagosomal Rupture by Mycobacterium Tuberculosis Results in Toxicity and Host Cell Death. PLoS Pathog. 2012, 8, e1002507. [Google Scholar] [CrossRef] [PubMed]
- Majlessi, L.; Prados-Rosales, R.; Casadevall, A.; Brosch, R. Release of Mycobacterial Antigens. Immunol. Rev. 2015, 264, 25–45. [Google Scholar] [CrossRef]
- Fortune, S.M.; Jaeger, A.; Sarracino, D.A.; Chase, M.R.; Sassetti, C.M.; Sherman, D.R.; Bloom, B.R.; Rubin, E.J. Mutually Dependent Secretion of Proteins Required for Mycobacterial Virulence. Proc. Natl. Acad. Sci. USA 2005, 102, 10676–10681. [Google Scholar] [CrossRef]
- Houben, D.; Demangel, C.; van Ingen, J.; Perez, J.; Baldeón, L.; Abdallah, A.M.; Caleechurn, L.; Bottai, D.; van Zon, M.; de Punder, K.; et al. ESX-1-Mediated Translocation to the Cytosol Controls Virulence of Mycobacteria. Cell. Microbiol. 2012, 14, 1287–1298. [Google Scholar] [CrossRef]
- Arend, S.M.; de Haas, P.; Leyten, E.; Rosenkrands, I.; Rigouts, L.; Andersen, P.; Mijs, W.; van Dissel, J.T.; van Soolingen, D. ESAT-6 and CFP-10 in Clinical versus Environmental Isolates of Mycobacterium Kansasii. J. Infect. Dis. 2005, 191, 1301–1310. [Google Scholar] [CrossRef][Green Version]
- Goy, G.; Thomas, V.; Rimann, K.; Jaton, K.; Prod’hom, G.; Greub, G. The Neff Strain of Acanthamoeba Castellanii, a Tool for Testing the Virulence of Mycobacterium Kansasii. Res. Microbiol. 2007, 158, 393–397. [Google Scholar] [CrossRef]
- Soucy, S.M.; Huang, J.; Gogarten, J.P. Horizontal Gene Transfer: Building the Web of Life. Nat. Rev. Genet. 2015, 16, 472–482. [Google Scholar] [CrossRef]
- Gagneux, S. Ecology and Evolution of Mycobacterium Tuberculosis. Nat. Rev. Microbiol. 2018, 16, 202–213. [Google Scholar] [CrossRef]
- Boritsch, E.C.; Khanna, V.; Pawlik, A.; Honoré, N.; Navas, V.H.; Ma, L.; Bouchier, C.; Seemann, T.; Supply, P.; Stinear, T.P.; et al. Key Experimental Evidence of Chromosomal DNA Transfer among Selected Tuberculosis-Causing Mycobacteria. Proc. Natl. Acad. Sci. USA 2016, 113, 9876–9881. [Google Scholar] [CrossRef]
- Tsukamura, M.; Hasimoto, M.; Noda, Y. Transformation of Isoniazid and Streptomycin Resistance in Mycobacterium Avium by the Desoxyribonucleate Derived from Isoniazid- and Streptomycin-Double-Resistant Cultures. Am. Rev. Respir. Dis. 1960, 81, 403–406. [Google Scholar] [CrossRef]
- Norgard, M.V.; Imaeda, T. Physiological Factors Involved in the Transformation of Mycobacterium Smegmatis. J. Bacteriol. 1978, 133, 1254–1262. [Google Scholar] [CrossRef]
- Gray, T.A.; Derbyshire, K.M. Blending Genomes: Distributive Conjugal Transfer in Mycobacteria, a Sexier Form of HGT. Mol. Microbiol. 2018, 108, 601–613. [Google Scholar] [CrossRef]
- Hatfull, G.F.; Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science Program; KwaZulu-Natal Research Institute for Tuberculosis and HIV Mycobacterial Genetics Course Students; Phage Hunters Integrating Research and Education Program. Complete Genome Sequences of 138 Mycobacteriophages. J. Virol. 2012, 86, 2382–2384. [Google Scholar] [CrossRef]
- Basra, S.; Anany, H.; Brovko, L.; Kropinski, A.M.; Griffiths, M.W. Isolation and Characterization of a Novel Bacteriophage against Mycobacteriumavium Subspecies Paratuberculosis. Arch. Virol. 2014, 159, 2659–2674. [Google Scholar] [CrossRef]
- Ummels, R.; Abdallah, A.M.; Kuiper, V.; Aâjoud, A.; Sparrius, M.; Naeem, R.; Spaink, H.P.; van Soolingen, D.; Pain, A.; Bitter, W. Identification of a Novel Conjugative Plasmid in Mycobacteria That Requires Both Type IV and Type VII Secretion. mBio 2014, 5, e01744-14. [Google Scholar] [CrossRef] [PubMed]
- da Rabello, M.C.S.; Matsumoto, C.K.; de Almeida, L.G.P.; Menendez, M.C.; de Oliveira, R.S.; Silva, R.M.; Garcia, M.J.; Leão, S.C. First Description of Natural and Experimental Conjugation between Mycobacteria Mediated by a Linear Plasmid. PLoS ONE 2012, 7, e29884. [Google Scholar] [CrossRef]
- Stinear, T.P.; Pryor, M.J.; Porter, J.L.; Cole, S.T. Functional Analysis and Annotation of the Virulence Plasmid PMUM001 from Mycobacterium Ulcerans. Microbiology 2005, 151, 683–692. [Google Scholar] [CrossRef]
- Mizuguchi, Y.; Suga, K.; Tokunaga, T. Multiple Mating Types of Mycobacterium Smegmatis. Jpn. J. Microbiol. 1976, 20, 435–443. [Google Scholar] [CrossRef] [PubMed]
- Gray, T.A.; Krywy, J.A.; Harold, J.; Palumbo, M.J.; Derbyshire, K.M. Distributive Conjugal Transfer in Mycobacteria Generates Progeny with Meiotic-like Genome-Wide Mosaicism, Allowing Mapping of a Mating Identity Locus. PLoS Biol. 2013, 11, e1001602. [Google Scholar] [CrossRef]
- Wang, J.; Karnati, P.K.; Takacs, C.M.; Kowalski, J.C.; Derbyshire, K.M. Chromosomal DNA Transfer in Mycobacterium Smegmatis Is Mechanistically Different from Classical Hfr Chromosomal DNA Transfer. Mol. Microbiol. 2005, 58, 280–288. [Google Scholar] [CrossRef]
- Campbell, I. Chi-Squared and Fisher-Irwin Tests of Two-by-Two Tables with Small Sample Recommendations. Stat. Med. 2007, 26, 3661–3675. [Google Scholar] [CrossRef]
- Diagnosis and Treatment of Disease Caused by Nontuberculous Mycobacteria. Am. J. Respir. Crit. Care Med. 1997, 156, S1–S25. [CrossRef] [PubMed]
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Pham, S.; Prjibelski, A.D.; et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef] [PubMed]
- Rissman, A.I.; Mau, B.; Biehl, B.S.; Darling, A.E.; Glasner, J.D.; Perna, N.T. Reordering Contigs of Draft Genomes Using the Mauve Aligner. Bioinformatics 2009, 25, 2071–2073. [Google Scholar] [CrossRef] [PubMed]
- Seemann, T. Prokka: Rapid Prokaryotic Genome Annotation. Bioinformatics 2014, 30, 2068–2069. [Google Scholar] [CrossRef] [PubMed]
- Tagini, F.; Pillonel, T.; Croxatto, A.; Bertelli, C.; Koutsokera, A.; Lovis, A.; Greub, G. Distinct Genomic Features Characterize Two Clades of Corynebacterium Diphtheriae: Proposal of Corynebacterium Diphtheriae Subsp. Diphtheriae Subsp. Nov. and Corynebacterium Diphtheriae Subsp. Lausannense Subsp. Nov. Front. Microbiol. 2018, 9, 1743. [Google Scholar] [CrossRef]
- Altschul, S.F.; Madden, T.L.; Schäffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleic Acids Res. 1997, 25, 3389–3402. [Google Scholar] [CrossRef]
- Galperin, M.Y.; Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Expanded Microbial Genome Coverage and Improved Protein Family Annotation in the COG Database. Nucleic Acids Res. 2015, 43, D261–D269. [Google Scholar] [CrossRef]
- Kanehisa, M.; Sato, Y.; Morishima, K. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J. Mol. Biol. 2016, 428, 726–731. [Google Scholar] [CrossRef] [PubMed]
- Jones, P.; Binns, D.; Chang, H.-Y.; Fraser, M.; Li, W.; McAnulla, C.; McWilliam, H.; Maslen, J.; Mitchell, A.; Nuka, G.; et al. InterProScan 5: Genome-Scale Protein Function Classification. Bioinformatics 2014, 30, 1236–1240. [Google Scholar] [CrossRef]
- Emms, D.M.; Kelly, S. OrthoFinder: Solving Fundamental Biases in Whole Genome Comparisons Dramatically Improves Orthogroup Inference Accuracy. Genome Biol. 2015, 16, 157. [Google Scholar] [CrossRef]
- Katoh, K.; Standley, D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013, 30, 772–780. [Google Scholar] [CrossRef]
- Stamatakis, A. RAxML Version 8: A Tool for Phylogenetic Analysis and Post-Analysis of Large Phylogenies. Bioinformatics 2014, 30, 1312–1313. [Google Scholar] [CrossRef]
- Mao, X.; Ma, Q.; Zhou, C.; Chen, X.; Zhang, H.; Yang, J.; Mao, F.; Lai, W.; Xu, Y. DOOR 2.0: Presenting Operons and Their Functions through Dynamic and Integrated Views. Nucleic Acids Res. 2014, 42, D654–D659. [Google Scholar] [CrossRef]
- Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree 2--Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE 2010, 5, e9490. [Google Scholar] [CrossRef]
- Collins, C.; Didelot, X. A Phylogenetic Method to Perform Genome-Wide Association Studies in Microbes That Accounts for Population Structure and Recombination. PLoS Comput. Biol. 2018, 14, e1005958. [Google Scholar] [CrossRef]
- Treangen, T.J.; Ondov, B.D.; Koren, S.; Phillippy, A.M. The Harvest Suite for Rapid Core-Genome Alignment and Visualization of Thousands of Intraspecific Microbial Genomes. Genome Biol. 2014, 15, 524. [Google Scholar] [CrossRef] [PubMed]
- Seemann, T. Snippy: Fast Bacterial Variant Calling from NGS Reads. Available online: https://github.com/tseemann/snippy (accessed on 8 February 2021).
- Forrellad, M.A.; Klepp, L.I.; Gioffré, A.; Sabio y García, J.; Morbidoni, H.R.; de la Paz Santangelo, M.; Cataldi, A.A.; Bigi, F. Virulence Factors of the Mycobacterium Tuberculosis Complex. Virulence 2013, 4, 3–66. [Google Scholar] [CrossRef] [PubMed]
- Simeone, R.; Bottai, D.; Frigui, W.; Majlessi, L.; Brosch, R. ESX/Type VII Secretion Systems of Mycobacteria: Insights into Evolution, Pathogenicity and Protection. Tuberculosis 2015, 95 (Suppl. 1), S150–S154. [Google Scholar] [CrossRef] [PubMed]
- Arndt, D.; Grant, J.R.; Marcu, A.; Sajed, T.; Pon, A.; Liang, Y.; Wishart, D.S. PHASTER: A Better, Faster Version of the PHAST Phage Search Tool. Nucleic Acids Res. 2016, 44, W16–W21. [Google Scholar] [CrossRef]
- Zhou, Y.; Liang, Y.; Lynch, K.H.; Dennis, J.J.; Wishart, D.S. PHAST: A Fast Phage Search Tool. Nucleic Acids Res. 2011, 39, W347–W352. [Google Scholar] [CrossRef]
- Guy, L.; Kultima, J.R.; Andersson, S.G.E. GenoPlotR: Comparative Gene and Genome Visualization in R. Bioinformatics 2010, 26, 2334–2335. [Google Scholar] [CrossRef] [PubMed]
- Abby, S.S.; Néron, B.; Ménager, H.; Touchon, M.; Rocha, E.P.C. MacSyFinder: A Program to Mine Genomes for Molecular Systems with an Application to CRISPR-Cas Systems. PLoS ONE 2014, 9, e110726. [Google Scholar] [CrossRef]
- Daleke, M.H.; Ummels, R.; Bawono, P.; Heringa, J.; Vandenbroucke-Grauls, C.M.J.E.; Luirink, J.; Bitter, W. General Secretion Signal for the Mycobacterial Type VII Secretion Pathway. Proc. Natl. Acad. Sci. USA 2012, 109, 11342–11347. [Google Scholar] [CrossRef] [PubMed]
- Kelley, L.A.; Mezulis, S.; Yates, C.M.; Wass, M.N.; Sternberg, M.J.E. The Phyre2 Web Portal for Protein Modeling, Prediction and Analysis. Nat. Protoc. 2015, 10, 845–858. [Google Scholar] [CrossRef] [PubMed]
- McLaughlin, B.; Chon, J.S.; MacGurn, J.A.; Carlsson, F.; Cheng, T.L.; Cox, J.S.; Brown, E.J. A Mycobacterium ESX-1-Secreted Virulence Factor with Unique Requirements for Export. PLoS Pathog. 2007, 3, e105. [Google Scholar] [CrossRef]
- Makarova, K.S.; Wolf, Y.I.; Alkhnbashi, O.S.; Costa, F.; Shah, S.A.; Saunders, S.J.; Barrangou, R.; Brouns, S.J.J.; Charpentier, E.; Haft, D.H.; et al. An Updated Evolutionary Classification of CRISPR–Cas Systems. Nat. Rev. Microbiol. 2015, 13, 722. [Google Scholar] [CrossRef]
- da Silva Telles, M.A.; Chimara, E.; Ferrazoli, L.; Riley, L.W. Mycobacterium Kansasii: Antibiotic Susceptibility and PCR-Restriction Analysis of Clinical Isolates. J. Med. Microbiol. 2005, 54, 975–979. [Google Scholar] [CrossRef] [PubMed]
- Santin, M.; Alcaide, F.; Benitez, M.A.; Salazar, A.; Ardanuy, C.; Podzamczer, D.; Rufi, G.; Dorca, J.; Martin, R.; Gudiol, F. Incidence and Molecular Typing of Mycobacterium Kansasii in a Defined Geographical Area in Catalonia, Spain. Epidemiol. Infect. 2004, 132, 425–432. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Mann, L.B.; Wilson, R.W.; Brown-Elliott, B.A.; Vincent, V.; Iinuma, Y.; Wallace, R.J. Molecular Analysis of Mycobacterium Kansasii Isolates from the United States. J. Clin. Microbiol. 2004, 42, 119–125. [Google Scholar] [CrossRef]
- Bakuła, Z.; Safianowska, A.; Nowacka-Mazurek, M.; Bielecki, J.; Jagielski, T. Short Communication: Subtyping of Mycobacterium Kansasii by PCR-Restriction Enzyme Analysis of the Hsp65 Gene. BioMed Res. Int. 2013, 2013, 178725. [Google Scholar] [CrossRef]
- Chen, J.M.; Zhang, M.; Rybniker, J.; Basterra, L.; Dhar, N.; Tischler, A.D.; Pojer, F.; Cole, S.T. Phenotypic Profiling of Mycobacterium Tuberculosis EspA Point Mutants Reveals That Blockage of ESAT-6 and CFP-10 Secretion In Vitro Does Not Always Correlate with Attenuation of Virulence. J. Bacteriol. 2013, 195, 5421–5430. [Google Scholar] [CrossRef]
- Chen, J.M.; Boy-Röttger, S.; Dhar, N.; Sweeney, N.; Buxton, R.S.; Pojer, F.; Rosenkrands, I.; Cole, S.T. EspD Is Critical for the Virulence-Mediating ESX-1 Secretion System in Mycobacterium Tuberculosis. J. Bacteriol. 2012, 194, 884–893. [Google Scholar] [CrossRef]
- Ates, L.S.; Brosch, R. Discovery of the Type VII ESX-1 Secretion Needle? Mol. Microbiol. 2017, 103, 7–12. [Google Scholar] [CrossRef] [PubMed]
- Broset, E.; Martín, C.; Gonzalo-Asensio, J. Evolutionary Landscape of the Mycobacterium Tuberculosis Complex from the Viewpoint of PhoPR: Implications for Virulence Regulation and Application to Vaccine Development. mBio 2015, 6, e01289-15. [Google Scholar] [CrossRef]
- Rohde, K.H.; Abramovitch, R.B.; Russell, D.G. Mycobacterium Tuberculosis Invasion of Macrophages: Linking Bacterial Gene Expression to Environmental Cues. Cell Host Microbe 2007, 2, 352–364. [Google Scholar] [CrossRef] [PubMed]
- Homolka, S.; Niemann, S.; Russell, D.G.; Rohde, K.H. Functional Genetic Diversity among Mycobacterium Tuberculosis Complex Clinical Isolates: Delineation of Conserved Core and Lineage-Specific Transcriptomes during Intracellular Survival. PLoS Pathog. 2010, 6, e1000988. [Google Scholar] [CrossRef] [PubMed]
- Ma, Z.; Strickland, K.T.; Cherne, M.D.; Sehanobish, E.; Rohde, K.H.; Self, W.T.; Davidson, V.L. The Rv2633c Protein of Mycobacterium Tuberculosis Is a Non-Heme Di-Iron Catalase with a Possible Role in Defenses against Oxidative Stress. J. Biol. Chem. 2018, 293, 1590–1595. [Google Scholar] [CrossRef]
- Huynen, M.; Snel, B.; Lathe, W.; Bork, P. Predicting Protein Function by Genomic Context: Quantitative Evaluation and Qualitative Inferences. Genome Res. 2000, 10, 1204–1210. [Google Scholar] [CrossRef]
- Sievers, F.; Wilm, A.; Dineen, D.; Gibson, T.J.; Karplus, K.; Li, W.; Lopez, R.; McWilliam, H.; Remmert, M.; Söding, J.; et al. Fast, Scalable Generation of High-quality Protein Multiple Sequence Alignments Using Clustal Omega. Mol. Syst. Biol. 2011, 7. [Google Scholar] [CrossRef]
- Kurtz, S.; Phillippy, A.; Delcher, A.L.; Smoot, M.; Shumway, M.; Antonescu, C.; Salzberg, S.L. Versatile and Open Software for Comparing Large Genomes. Genome Biol. 2004, 5, R12. [Google Scholar] [CrossRef]
- Delcher, A.L.; Phillippy, A.; Carlton, J.; Salzberg, S.L. Fast Algorithms for Large-Scale Genome Alignment and Comparison. Nucleic Acids Res. 2002, 30, 2478–2483. [Google Scholar] [CrossRef]
Strain ID | Spec. | Age | Diagnosis | Co-Morbidities | P. | I. | O. | Species | Or. |
---|---|---|---|---|---|---|---|---|---|
1010001468 | Environm. | NA | NA | NA | 4 | NA | 0 | M. attenuatum | 0 |
MK136 | ND | ND | Colonization | ND | 5 | ND | 0 | M. attenuatum | 1 |
MK191 | ND | ND | Colonization | ND | 5 | ND | 0 | M. attenuatum | 1 |
MK41 | Bronch. asp. | 48 | Colonization | Lung transplanted | 5 | 1 | 0 | M. attenuatum | 2 |
NLA001001166 | ND | ND | Colonization | Bronchectasis | 4 | ND | 0 | M. attenuatum | 0 |
1010001458 | Environm. | NA | NA | NA | 4 | NA | 0 | M. ostraviense | 0 |
DSM43505 | Gastric lavage | ND | Colonization | ND | 4 | ND | 0 | M. gastri | 0 |
1010001454 | Environm. | NA | NA | NA | 4 | NA | 0 | M. innocens | 0 |
1010001493 | Environm. | NA | NA | NA | 4 | NA | 0 | M. innocens | 0 |
MK13 | Sputum | 87 | ND | ND | 3 | ND | 0 | M. innocens | 2 |
662 | BAL/Bronch. asp. | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
824 | Sputum | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
1010001495 | Environm. | NA | NA | NA | 4 | NA | 0 | M. kansasii | 0 |
10 MK | Sputum | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
11 MK | BAL | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
1 MK | Sputum | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
4MK | Sputum | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
5MK | BAL | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
6MK | Sputum | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
9MK | BAL | ND | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
ATCC12478 | ND | ND | NTM disease | ND | 2 | ND | 0 | M. kansasii | 0 |
MK1 | BAL | 50 | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 2 |
MK12 | Sputum | 19 | Lung NTM disease | - | 1 | 1 | 0 | M. kansasii | 2 |
MK135 | ND | ND | Lung NTM disease | ND | 1 | ND | 0 | M. kansasii | 1 |
MK156 | ND | ND | Lung NTM disease | ND | 1 | ND | 0 | M. kansasii | 1 |
MK17 | Bronch. asp. | 71 | Lung NTM disease | Lung adenocarcinoma, bronchectasis | 1 | 0 | 0 | M. kansasii | 2 |
MK18 | Bronch. asp. | 67 | ND | ND | 3 | ND | 0 | M. kansasii | 2 |
MK186 | ND | ND | Lung NTM disease | ND | 1 | ND | 0 | M. kansasii | 1 |
MK19 | Sputum | 68 | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 2 |
MK190 | ND | ND | Lung NTM disease | ND | 1 | ND | 0 | M. kansasii | 1 |
MK20 | Sputum | 16 | Colonization | Cystic fibrosis | 5 | 0 | 0 | M. kansasii | 2 |
MK22 | Biopsy | 27 | Tenosynovitis, flexor of the 3rd finger | History of toxic pneumonitis due to hydrogen chroride exposition | 1 | 0 | 1 | M. kansasii | 2 |
MK26 | Biopsy | 23 | Finger infection (no further information) | ND | 1 | ND | 1 | M. kansasii | 2 |
MK28 | Bronch. asp. | 64 | ND | ND | 3 | ND | 0 | M. kansasii | 2 |
MK29 | BAL | 58 | ND | ND | 2 | ND | 0 | M. kansasii | 2 |
MK3 | BAL | 77 | ND | Lung adenocarcinoma | 4 | 0 | 0 | M. kansasii | 2 |
MK30 | Bronch. asp. | 67 | Colonization | Lung adenocarcinoma, COPD, liver cirrhosis, valvular and rythmic cardiopathy | 5 | 0 | 0 | M. kansasii | 2 |
MK31 | Bronch. asp. | 63 | ND | Rhumatoid arthritis | 3 | 1 | 0 | M. kansasii | 2 |
MK34 | Sputum | 82 | Lung NTM disease | Rhumatoid arthritis with lung involvement | 1 | 1 | 0 | M. kansasii | 2 |
MK36 | Sputum | 59 | Colonization | Primary ciliary dyskinesia, bronchectasis | 5 | 0 | 0 | M. kansasii | 2 |
MK38 | Surgical spec. | 47 | Sternitis | Rhumatoid arthritis | 1 | 1 | 1 | M. kansasii | 2 |
MK39 | Sputum | 49 | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 2 |
MK40 | Surgical spec. | 49 | Hand infection (no further information) | Chronic hip prosthesis infection with Propionibacterium acnes | 1 | 0 | 1 | M. kansasii | 2 |
MK5 | Sputum | 32 | Lung NTM disease | ND | 2 | ND | 0 | M. kansasii | 2 |
MK52 | Sputum | 66 | Colonization | Lung adenocarcinoma, COPD | 5 | 0 | 0 | M. kansasii | 2 |
MK6 | Sputum | 73 | ND | ND | 3 | ND | 0 | M. kansasii | 2 |
MK7 | Sputum | 34 | Lung NTM disease | Chronic hepatitis B treated with alfa-2a peginterferon | 1 | 1 | 0 | M. kansasii | 2 |
MK83 | ND | ND | Lung NTM disease | ND | 1 | ND | 0 | M. kansasii | 1 |
SMC1 | ND | ND | Human-environ. | ND | 3 | ND | 0 | M. kansasii | 0 |
1010001469 | Environm. | NA | NA | NA | 4 | NA | 0 | M. persicum | 0 |
12MK | BAL | ND | Colonization | ND | 4 | ND | 0 | M. persicum | 0 |
3MK | BAL | ND | Colonization | ND | 4 | ND | 0 | M. persicum | 0 |
7MK | Sputum | ND | Colonization | ND | 4 | ND | 0 | M. persicum | 0 |
8MK | BAL | ND | Colonization | ND | 4 | ND | 0 | M. persicum | 0 |
MK15 | Endotracheal secretions | 8 | Colonization | Still’s disease | 5 | 1 | 0 | M. persicum | 2 |
MK16 | Sputum | 29 | Colonization | Disseminated M. avium infection | 3 | 1 | 0 | M. persicum | 2 |
MK4 | Bronch. asp. | 28 | NTM disease | Acute lymphoblastic leukemia, bone marrow allografted | 1 | 1 | 0 | M. persicum | 2 |
MK42 | Surgical spec. | 32 | Chronic olecranon bursitis | ND | 1 | ND | 1 | M. persicum | 2 |
MK47 | Bronch. asp. | 77 | Lung NTM disease | Polymyalgia rhumatica | 1 | 1 | 0 | M. persicum | 2 |
MK53 | Sputum | 76 | ND | ND | 3 | ND | 0 | M. persicum | 2 |
MK54 | Bronch. asp. | 27 | Colonization | Bronchectasis | 5 | 0 | 0 | M. persicum | 2 |
MK11 | Urine | 27 | Colonization | Recurent UTI | 3 | 0 | 0 | M. pseudokansasii | 2 |
MK123 | ND | ND | Colonization | ND | 5 | ND | 0 | M. pseudokansasii | 1 |
MK142 | Blood culture | ND | Bacteremia, disseminated disease | ND | 1 | ND | 0 | M. pseudokansasii | 1 |
MK151 | ND | ND | Colonization | ND | 5 | ND | 0 | M. pseudokansasii | 1 |
MK21 | Sputum | 52 | Colonization | History of community-acquired pneumococcal pneumonia | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK32 | Sputum | 80 | Colonization | Small cell lung carcinoma, history of radiation pneumonitis and M. tuberculosis infection | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK33 | Bronch. asp. | 60 | Colonization | Small cell lung carcinoma | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK35 | Sputum | 47 | Colonization | History of M. tuberculosis infection, Barret’s oesophagus, rectal adenocarcinoma | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK43 | Bronch. asp. | 9 | Colonization | Miller-Dieker syndrome | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK46 | Sputum | 30 | Colonization | History of M. tuberculosis infecction | 5 | 0 | 0 | M. pseudokansasii | 2 |
MK48 | Sputum | 33 | ND | ND | 3 | ND | 0 | M. pseudokansasii | 2 |
MK75 | ND | ND | Colonization | ND | 5 | ND | 0 | M. pseudokansasii | 1 |
MK8 | Urine | 51 | UTI | Renal transplanted | 1 | 1 | 0 | M. pseudokansasii | 2 |
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Tagini, F.; Pillonel, T.; Bertelli, C.; Jaton, K.; Greub, G. Pathogenic Determinants of the Mycobacterium kansasii Complex: An Unsuspected Role for Distributive Conjugal Transfer. Microorganisms 2021, 9, 348. https://doi.org/10.3390/microorganisms9020348
Tagini F, Pillonel T, Bertelli C, Jaton K, Greub G. Pathogenic Determinants of the Mycobacterium kansasii Complex: An Unsuspected Role for Distributive Conjugal Transfer. Microorganisms. 2021; 9(2):348. https://doi.org/10.3390/microorganisms9020348
Chicago/Turabian StyleTagini, Florian, Trestan Pillonel, Claire Bertelli, Katia Jaton, and Gilbert Greub. 2021. "Pathogenic Determinants of the Mycobacterium kansasii Complex: An Unsuspected Role for Distributive Conjugal Transfer" Microorganisms 9, no. 2: 348. https://doi.org/10.3390/microorganisms9020348
APA StyleTagini, F., Pillonel, T., Bertelli, C., Jaton, K., & Greub, G. (2021). Pathogenic Determinants of the Mycobacterium kansasii Complex: An Unsuspected Role for Distributive Conjugal Transfer. Microorganisms, 9(2), 348. https://doi.org/10.3390/microorganisms9020348