Clonal diversification and changes in lipid traits and colony morphology in mycobacterium abscessus clinical isolates

Journal of Clinical Microbiology

Volumn 53, Issue 11, 2015, Pages 3438-3447

  Park, In Kwon ^a   Hsu, Amy P ^a   Tettelin, Hervé ^b   Shallom, Shamira J ^c   Drake, Steven K ^c   Ding, Li ^a   Wu, Un In ^a   Adamo, Nick ^a   Rebecca Prevots, D ^a   Olivier, Kenneth N ^d   Holland, Steven M ^a   Sampaio, Elizabeth P ^a,e   Zelazny, Adrian M ^a,c  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOLIPID; GLYCOPEPTIDOLIPID; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; LIGASE; LIPID; RNA 16S;

ACID FAST BACTERIUM; ADULT; AGED; ARTICLE; BACTERIAL GENE; BACTERIUM COLONY; BACTERIUM ISOLATE; CLINICAL ARTICLE; CLONAL VARIATION; FADD23 GENE; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HUMAN; LUNG INFECTION; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MIDDLE AGED; MMPL4A GENE; MMPS4 GENE; MPS1 GENE; MPS2 GENE; MULTILOCUS SEQUENCE TYPING; MYCOBACTERIOSIS; MYCOBACTERIUM ABSCESSUS; NONHUMAN; PRIORITY JOURNAL; THIN LAYER CHROMATOGRAPHY; VERY ELDERLY; ATYPICAL MYCOBACTERIOSIS; ATYPICAL MYCOBACTERIUM; BACTERIAL GENOME; BRONCHIECTASIS; CLASSIFICATION; CYSTIC FIBROSIS; DNA SEQUENCE; GENE DOSAGE; GENETICS; ISOLATION AND PURIFICATION; LIPID METABOLISM; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; MICROBIOLOGY; NUCLEOTIDE SEQUENCE;

AGED; AGED, 80 AND OVER; BACTERIAL PROTEINS; BASE SEQUENCE; BRONCHIECTASIS; CYSTIC FIBROSIS; DNA, BACTERIAL; FEMALE; GENE DOSAGE; GENOME, BACTERIAL; HUMANS; LIGASES; LIPID METABOLISM; LIPIDS; MALE; MIDDLE AGED; MULTILOCUS SEQUENCE TYPING; MYCOBACTERIUM INFECTIONS, NONTUBERCULOUS; NONTUBERCULOUS MYCOBACTERIA; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84945241874     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02015-15     Document Type: Article

References (35)

1. Adekambi T, Reynaud-Gaubert M, Greub G, Gevaudan MJ, La Scola B, Raoult D, Drancourt M. 2004. Amoebal coculture of "Mycobacterium massiliense" sp. nov. from the sputum of a patient with hemoptoic pneumonia. JClin Microbiol 42:5493-5501. http://dx.doi.org/10.1128/JCM.42.12.5493-5501.2004.
2. Adekambi T, Berger P, Raoult D, Drancourt M. 2006. rpoB gene sequence-based characterization of emerging non-tuberculous mycobacte-ria with descriptions of Mycobacterium bolletii sp. nov., Mycobacterium phocaicum sp. nov. and Mycobacterium aubagnense sp. nov. Int J Syst Evol Microbiol 56:133-143. http://dx.doi.org/10.1099/ijs.0.63969-0.
3. Zelazny AM, Root JM, Shea YR, Colombo RE, Shamputa IC, Stock F, Conlan S, McNulty S, Brown-Elliott BA, Wallace RJ, Jr, Olivier KN, Holland SM, Sampaio EP. 2009. Cohort study of molecular identification and typing of Mycobacterium abscessus, Mycobacterium massiliense, and Mycobacterium bolletii. J Clin Microbiol 47:1985-1995. http://dx.doi.org/10.1128/JCM.01688-08.
4. Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, Reacher M, Haworth CS, Curran MD, Harris SR, Peacock SJ, Parkhill J, Floto RA. 2013. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 381:1551-1560. http://dx.doi.org/10.1016/S0140-6736(13)60632-7.
5. Tettelin H, Davidson RM, Agrawal S, Aitken ML, Shallom S, Hasan NA, Strong M, de Moura VC, De Groote MA, Duarte RS, Hine E, Parankush S, Su Q, Daugherty SC, Fraser CM, Brown-Elliott BA, Wallace RJ, Jr, Holland SM, Sampaio EP, Olivier KN, Jackson M, Zelazny AM. 2014. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks Emerg Infect Dis 20:364-371.
6. Leung JM, Olivier KN. 2013. Nontuberculous mycobacteria: the changing epidemiology and treatment challenges in cystic fibrosis. Curr Opin Pulm Med 19:662-669. http://dx.doi.org/10.1097/MCP.0b013e328365ab33.
7. Jang MA, Koh WJ, Huh HJ, Kim SY, Jeon K, Ki CS, Lee NY. 2014. Distribution of nontuberculous mycobacteria by multigene sequence-based typing and clinical significance of isolated strains. J Clin Microbiol 52:1207-1212. http://dx.doi.org/10.1128/JCM.03053-13.
8. Qvist T, Gilljam M, Jonsson B, Taylor-Robinson D, Jensen-Fangel S, Wang M, Svahn A, Kotz K, Hansson L, Hollsing A, Hansen CR, Finstad PL, Pressler T, Hoiby N, Katzenstein TL, Scandinavian Cystic Fibrosis Study Consortium. 2015. Epidemiology of nontuberculous mycobacteria among patients with cystic fibrosis in Scandinavia. JCyst Fibros 14:46-52. http://dx.doi.org/10.1016/j.jcf.2014.08.002.
9. Ripoll F, Deshayes C, Pasek S, Laval F, Beretti JL, Biet F, Risler JL, Daffe M, Etienne G, Gaillard JL, Reyrat JM. 2007. Genomics of glycopeptido-lipid biosynthesis in Mycobacterium abscessus and M. chelonae. BMC Genomics 8:114. http://dx.doi.org/10.1186/1471-2164-8-114.
10. Howard ST, Rhoades E, Recht J, Pang X, Alsup A, Kolter R, Lyons CR, Byrd TF. 2006. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology 152:1581-1590. http://dx.doi.org/10.1099/mic.0.28625-0.
11. Catherinot E, Clarissou J, Etienne G, Ripoll F, Emile JF, Daffe M, Perronne C, Soudais C, Gaillard JL, Rottman M. 2007. Hypervirulence of a rough variant of the Mycobacterium abscessus type strain. Infect Im-mun 75:1055-1058. http://dx.doi.org/10.1128/IAI.00835-06.
12. Catherinot E, Roux AL, Macheras E, Hubert D, Matmar M, Dannhoffer L, Chinet T, Morand P, Poyart C, Heym B, Rottman M, Gaillard JL, Herrmann JL. 2009. Acute respiratory failure involving an R variant of Mycobacterium abscessus. J Clin Microbiol 47:271-274. http://dx.doi.org/10.1128/JCM.01478-08.
13. Jonsson B, Ridell M, Wold AE. 2013. Phagocytosis and cytokine response to rough and smooth colony variants of Mycobacterium abscessus by human peripheral blood mononuclear cells. APMIS 121:45-55. http://dx.doi.org/10.1111/j.1600-0463.2012.02932.x.
14. Bernut A, Herrmann JL, Kissa K, Dubremetz JF, Gaillard JL, Lutfalla G, Kremer L. 2014. Mycobacterium abscessus cording prevents phagocytosis and promotes abscess formation. Proc Natl Acad Sci USA 111:E943-E952. http://dx.doi.org/10.1073/pnas.1321390111.
15. Caverly LJ, Caceres SM, Fratelli C, Happoldt C, Kidwell KM, Malcolm KC, Nick JA, Nichols DP. 2015. Mycobacterium abscessus morphotype comparison in a murine model. PLoS One 10:e0117657. http://dx.doi.org/10.1371/journal.pone.0117657.
16. Kreutzfeldt KM, McAdam PR, Claxton P, Holmes A, Seagar AL, Lau-renson IF, Fitzgerald JR. 2013. Molecular longitudinal tracking of Myco-bacterium abscessusspp. during chronic infection ofthe human lung. PLoS One 8:e63237. http://dx.doi.org/10.1371/journal.pone.0063237.
17. Tatham E, Sundaram Chavadi S, Mohandas P, Edupuganti UR, Angala SK, Chatterjee D, Quadri LE. 2012. Production of mycobacterial cell wall glycopeptidolipids requires a member of the MbtH-like protein family. BMC Microbiol 12:118. http://dx.doi.org/10.1186/1471-2180-12-118.
18. Zwadyk P, Jr, Down JA, Myers N, Dey MS. 1994. Rendering of myco-bacteria safe for molecular diagnostic studies and development of a lysis method for strand displacement amplification and PCR. J Clin Microbiol 32:2140-2146.
19. Pathak S, Awuh JA, Leversen NA, Flo TH, Asjo B. 2012. Counting mycobacteria in infected human cells and mouse tissue: a comparison between qPCR and CFU. PLoS One 7:e34931. http://dx.doi.org/10.1371/journal.pone.0034931.
20. Bansal-Mutalik R, Nikaido H. 2014. Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phospha-tidylinositol dimannosides. Proc Natl Acad Sci USA 111:4958-4963. http://dx.doi.org/10.1073/pnas.1403078111.
21. Kuksis A. 2004. Lipids, p 770-771. In Heftmann E (ed), Chromatogra-phy: fundamentals and applications of chromatography and related differential migration methods, 6th ed, vol 69B. Elsevier B.V., Amsterdam The Netherlands.
22. Pawlik A, Garnier G, Orgeur M, Tong P, Lohan A, Le Chevalier F, Sapriel G, Roux AL, Conlon K, Honore N, Dillies MA, Ma L, Bouchier C, Coppee JY, Gaillard JL, Gordon SV, Loftus B, Brosch R, Herrmann JL. 2013. Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clinically persistent Mycobacterium abscessus. Mol Microbiol 90:612-629. http://dx.doi.org/10.1111/mmi.12387.
23. Sonden B, Kocincova D, Deshayes C, Euphrasie D, Rhayat L, Laval F, Frehel C, Daffe M, Etienne G, Reyrat JM. 2005. Gap, a mycobacterial specific integral membrane protein, is required for glycolipid transport to the cell surface. Mol Microbiol 58:426-440. http://dx.doi.org/10.1111/j.1365-2958.2005.04847.x.
24. Deshayes C, Bach H, Euphrasie D, Attarian R, Coureuil M, Sougakoff W, Laval F, Av-Gay Y, Daffe M, Etienne G, Reyrat JM. 2010. MmpS4 promotes glycopeptidolipids biosynthesis and export in Mycobacterium smegmatis. Mol Microbiol 78:989-1003. http://dx.doi.org/10.1111/j.1365-2958.2010.07385.x.
25. Nessar R, Reyrat JM, Davidson LB, Byrd TF. 2011. Deletion of the mmpL4b gene in the Mycobacterium abscessus glycopeptidolipid biosyn-thetic pathway results in loss of surface colonization capability, but enhanced ability to replicate in human macrophages and stimulate their innate immune response. Microbiology 157:1187-1195. http://dx.doi.org/10.1099/mic.0.046557-0.
26. Daniel J, Deb C, Dubey VS, Sirakova TD, Abomoelak B, Morbidoni HR, Kolattukudy PE. 2004. Induction of a novel class of diacylglycerol acyltransferases and triacylglycerol accumulation in Mycobacterium tuberculosis as it goes into a dormancy-like state in culture. J Bacteriol 186: 5017-5030. http://dx.doi.org/10.1128/JB.186.15.5017-5030.2004.
27. Pandey AK, Sassetti CM. 2008. Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105:4376-4380. http://dx.doi.org/10.1073/pnas.0711159105.
28. Shi L, Sohaskey CD, Pfeiffer C, Datta P, Parks M, McFadden J, North RJ, Gennaro ML. 2010. Carbon flux rerouting during Mycobacterium tuberculosisgrowth arrest. Mol Microbiol 78:1199-1215. http://dx.doi.org/10.1111/j.1365-2958.2010.07399.x.
29. Baek SH, Li AH, Sassetti CM. 2011. Metabolic regulation of mycobac-terial growth and antibiotic sensitivity. PLoS Biol 9:e1001065. http://dx.doi.org/10.1371/journal.pbio.1001065.
30. Larrouy-Maumus G, Puzo G. 2015. Mycobacterial envelope lipids fingerprint from direct MALDI-TOF MS analysis of intact bacilli. Tuberculosis (Edinb) 95:75-85. http://dx.doi.org/10.1016/j.tube.2014.11.001.
31. Trivedi OA, Arora P, Sridharan V, Tickoo R, Mohanty D, Gokhale RS. 2004. Enzymic activation and transfer of fatty acids as acyl-adenylates in my-cobacteria. Nature 428:441-445. http://dx.doi.org/10.1038/nature02384.
32. Simeone R, Leger M, Constant P, Malaga W, Marrakchi H, Daffe M, Guilhot C, Chalut C. 2010. Delineation of the roles of FadD22, FadD26 and FadD29 in the biosynthesis of phthiocerol dimycocerosates and related compounds in Mycobacterium tuberculosis. FEBS J 277:2715-2725. http://dx.doi.org/10.1111/j.1742-4658.2010.07688.x.
33. O'Connell ML, Birkenkamp KE, Kleiner DE, Folio LR, Holland SM, Olivier KN. 2012. Lung manifestations in an autopsy-based series of pulmonary or disseminated nontuberculous mycobacterial disease. Chest 141:1203-1209. http://dx.doi.org/10.1378/chest.11-0425.
34. Lieberman TD, Flett KB, Yelin I, Martin TR, McAdam AJ, Priebe GP, Kishony R. 2014. Genetic variation of a bacterial pathogen within individuals with cystic fibrosis provides a record of selective pressures. Nat Genet 46:82-87. http://dx.doi.org/10.1038/ng.2848.
35. Shallom SJ, Moura NS, Olivier KN, Sampaio EP, Holland SM, Zelazny AM. 12 August 2015. New real-time PCR assays for detection of inducible and acquired clarithromycin resistance in the Mycobacterium abscessus group. J Clin Microbiol http://dx.doi.org/10.1128/JCM.01714-15.