Journal of Microbiology and Biotechnology

  • 제29권6호
  • /
  • Pages.887-896
  • /
  • 2019
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Reliable Identification of Bacillus cereus Group Species Using Low Mass Biomarkers by MALDI-TOF MS

  • 투고 : 2019.03.15
  • 심사 : 2019.06.03
  • 발행 : 2019.06.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS)-based pathogen identification relies on the ribosomal protein spectra provided in the proprietary database. Although these mass spectra can discern various pathogens at species level, the spectra-based method still has limitations in identifying closely-related microbial species. In this study, to overcome the limits of the current MALDI-TOF MS identification method using ribosomal protein spectra, we applied MALDI-TOF MS of low-mass profiling to the identification of two genetically related Bacillus species, the food-borne pathogen Bacillus cereus, and the insect pathogen Bacillus thuringiensis. The mass spectra of small molecules from 17 type strains of two bacilli were compared to the morphological, biochemical, and genetic identification methods of pathogens. The specific mass peaks in the low-mass range (m/z 500-3,000) successfully identified various closely-related strains belonging to these two reference species. The intensity profiles of the MALDI-TOF mass spectra clearly revealed the differences between the two genetically-related species at strain level. We suggest that small molecules with low molecular weight, 714.2 and 906.5 m/z can be potential mass biomarkers used for reliable identification of B. cereus and B. thuringiensis.

키워드

참고문헌

  1. Barbuddhe SB, Maier T, Schwarz G, Kostrzewa M, Hof H, Domann E, et al. 2008. Rapid identification and typing of listeria species by matrix-assisted laser desorption ionizationtime of flight mass spectrometry. Appl. Environ. Microbiol. 74: 5402-5407. https://doi.org/10.1128/AEM.02689-07
  2. Bessède E, Solecki O, Sifre E, Labadi L, Megraud F. 2011. Identification of Campylobacter species and related organisms by matrix assisted laser desorption ionization-time of flight (MALDI-TOF) mass spectrometry. Clin. Microbiol. Infect. 17: 1735-1739. https://doi.org/10.1111/j.1469-0691.2011.03468.x
  3. Bizzini A, Durussel C, Bille J, Greub G, Prod'hom G. 2010. Performance of matrix-assisted laser desorption ionizationtime of flight mass spectrometry for identification of bacterial strains routinely isolated in a clinical microbiology laboratory. J. Clin. Microbiol. 48: 1549-1554. https://doi.org/10.1128/JCM.01794-09
  4. Dieckmann R, Strauch E, Alter T. 2010. Rapid identification and characterization of Vibrio species using whole-cell MALDI-TOF mass spectrometry. J. Appl. Microbiol. 109: 199-211. https://doi.org/10.1111/j.1365-2672.2009.04647.x
  5. Grosse-Herrenthey A, Maier T, Gessler F, Schaumann R, Bohnel H, Kostrzewa M, et al. 2008. Challenging the problem of clostridial identification with matrix-assisted laser desorption and ionization-time-of-flight mass spectrometry (MALDI-TOF MS). Anaerobe 14: 242-249. https://doi.org/10.1016/j.anaerobe.2008.06.002
  6. Sparbier K, Weller U, Boogen C, Kostrewa M. 2010. Rapid detection of Salmonella sp. by means of a combination of selective enrichment broth and MALDITOF MS. Eur. J. Clin. Microbiol. Infect. Dis. 31: 767-773. https://doi.org/10.1007/s10096-011-1373-0
  7. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann S. 2010. Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J. Med. Microbiol. 59: 787-790. https://doi.org/10.1099/jmm.0.016733-0
  8. Petersen CE, Valentine NB, Wahl KL. 2009. Characterization of microorganisms by MALDI mass spectrometry. Methods Mol. Biol. 492: 367-379. https://doi.org/10.1007/978-1-59745-493-3_22
  9. Public Health England. 2015. UK standards for microbiology investigations (ID 9): Identification of Bacillus species, bacteriology-identification. 3: 1-27.
  10. Croxatto A, Prod'hom G, Greub G. 2012. Application of MALDI-TOF mass spectrometry in clinical diagnostic microbiology. FEMS Microbiol. Rev. 36: 380-407. https://doi.org/10.1111/j.1574-6976.2011.00298.x
  11. Seibold E, Maier T, Kostrzewa M, Zeman E, Splettstoesser W. 2010. Identification of Francisella tularensis by whole-cell matrix-assisted laser desorption ionization-time of flight mass spectrometry: Fast, reliable, robust, and cost-effective differentiation on species and subspecies levels. J. Clin. Microbiol. 48: 1061-1069. https://doi.org/10.1128/JCM.01953-09
  12. Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, et al. 2009. Ongoing revolution in bacteriology: Routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin. Infect. Dis. 49: 543-551. https://doi.org/10.1086/600885
  13. Ha M, Son EJ, Choi EJ. 2016. Application of MALDI-TOF mass spectrometry-based identification of foodborne pathogen tests to the Korea Food Standard Codex. Korean J. Food Sci. Technol. 48: 437-444. https://doi.org/10.9721/KJFST.2016.48.5.437
  14. Ryzhov V, Fenselau C. 2001. Characterization of the protein subset desorbed by MALDI from whole bacterial cells. Anal. Chem. 73: 746-750. https://doi.org/10.1021/ac0008791
  15. Bremer H, Dennis PP. 1996. Modulation of chemical composition and other parameters of the cell by growth rate. Cell. Mol. Biol., pp. 167-182. In Neidhardt FC (ed.), Escherichia coli and Salmonella. ASM Press, Washington, DC.
  16. Wieser A, Schneider L, Jung J, Schubert S. 2012. MALDITOF MS in microbiological diagnostics-identification of microorganisms and beyond (mini review). Appl. Microbiol. Biotechnol. 93: 965-974. https://doi.org/10.1007/s00253-011-3783-4
  17. McLaughlin J, Nelson M, McNevin D, Roffey P, Gahan ME. 2014. Characterization of Bacillus strains and hoax agents by protein profiling using automated microfluidic capillary electrophoresis. Forensic Sci. Med. Pathol. 10: 380-389. https://doi.org/10.1007/s12024-014-9578-z
  18. Fritze D. 2004. Taxonomy of the genus bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94: 1245-1248. https://doi.org/10.1094/PHYTO.2004.94.11.1245
  19. Ehling-Schulz M, Svensson B, Guinebretiere MH, Lindback T, Andersson M, Schulz A, et al. 2005. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 151(Pt. 1): 183-197. https://doi.org/10.1099/mic.0.27607-0
  20. Lindback T, Granum PE. 2006. Detection and purification of Bacillus cereus enterotoxins. In Adley, C. C., (Ed.), Foodborne Pathogens: Methods and Protocols, pp. 15-26. Humana Press, Totowa, NJ.
  21. Gaviria Rivera AMG, Granum PE, Priest FG. 2000. Common occurrence of enterotoxin genes and enterotoxicity in Bacillus thuringiensis. FEMS Microbiol. Lett. 190: 151-155. https://doi.org/10.1111/j.1574-6968.2000.tb09278.x
  22. Stenfors LP, Mayr R, Scherer S, Granum PE. 2002. Pathogenic potential of fifty Bacillus weihenstephanensis strains. FEMS Microbiol. Lett. 215: 47-51. https://doi.org/10.1111/j.1574-6968.2002.tb11368.x
  23. Ehling-Schultz M, Fricker M and Scherer S. 2004. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol. Nutr. Food Res. 48: 479-487. https://doi.org/10.1002/mnfr.200400055
  24. Schoeni JL, Wong AC. 2005. Bacillus cereus food poisoning and its toxins. J. Food Prot. 68: 636-648. https://doi.org/10.4315/0362-028X-68.3.636
  25. Van der Auwera GA, Timmery S, Hoton F, Mahillon J. 2007. Plasmid exchanges among members of the Bacillus cereus group in foodstuffs. Int. J. Food Microbiol. 113: 164-172. https://doi.org/10.1016/j.ijfoodmicro.2006.06.030
  26. Ullom JN, Frank M, Gard EE, Horn JM, Labov SE, Langry K, et al. 2001. Discrimination between bacterial spore types using time-of-flight mass spectrometry and matrix-free infrared laser desorption and ionization. Anal. Chem. 73: 2331-2337. https://doi.org/10.1021/ac001551a
  27. Aronson A. 2002. Sporulation and delta-endotoxin synthesis by Bacillus thuringiensis. Cell. Mol. Life Sci. 59: 417-425. https://doi.org/10.1007/s00018-002-8434-6
  28. Drobniewski FA. 1993. Bacillus cereus and related species. Clin. Microbiol. Rev. 6: 324-338. https://doi.org/10.1128/CMR.6.4.324
  29. Emmerson AM, Hawkey PM, Gillespie SH. 1997. Bacillus, Aliscylobacillus and Paenibacillus, pp. 185-207. In Berkeley RCW, Logan NA, editors. Principles and Practice of Clinical Bacteriology. Chichester: John Wiley & Sons.
  30. Helgason E, Okstad OA, Caugant DA, Johansen HA, Fouet A, Mock M, et al. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis-one species on the basis of genetic evidence. Appl. Environ. Microbiol. 66: 2627-2630. https://doi.org/10.1128/AEM.66.6.2627-2630.2000
  31. Punina NV, Zotov VS, Parkhomenko AL, Parkhomenko TU, Topunov AF. 2013. Genetic diversity of Bacillus thuringiensis from different geoecological regions of Ukraine by analyzing the 16S rRNA and gyrB genes and by AP-PCR and saAFLP. Acta Naturae 5: 90-100.
  32. Murray PR. 2010. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry: usefulness for taxonomy and epidemiology. Clin. Microbiol. Infect. 16: 1626-1630. https://doi.org/10.1111/j.1469-0691.2010.03364.x
  33. Klevan A, Tourasse NJ, Stabell FB, Kolsto AB, Okstad OA. 2007. Exploring the evolution of the Bacillus cereus group repeat element bcr1 by comparative genome analysis of closely related strains. Microbiology 153(Pt 11): 3894-908. https://doi.org/10.1099/mic.0.2007/005504-0
  34. Ash C, Farrow JA, Dorsch M, Stackebrandt E, Collins MD. 1991. Comparative analysis of Bacillus anthracis, Bacillus cereus, and related species on the basis of reverse transcriptase gene sequencing of 16S rRNA. Int. J. Syst. Bacteriol. 41: 343-346. https://doi.org/10.1099/00207713-41-3-343
  35. Alocilja EC and Radke SM. 2003. Market analysis of biosensors for food safety. Biosens Bioelectron. 18: 841-846. https://doi.org/10.1016/S0956-5663(03)00009-5
  36. Pal S, Alocilja EC and Downes FP. 2007. Nanowire labeled direct-charge transfer biosensor for detecting Bacillus species. Biosens. Bioelectron. 22: 2329-2336. https://doi.org/10.1016/j.bios.2007.01.013
  37. Halket G, Dinsdale AE, Logan NA. 2010. Evaluation of the VITEK2 BCL card for identification of Bacillus species and other aerobic endospore formers. Lett. Appl. Microbiol. 50: 120-126. https://doi.org/10.1111/j.1472-765X.2009.02765.x
  38. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173: 697-703. https://doi.org/10.1128/jb.173.2.697-703.1991
  39. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. 2008. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl. Environ. Microbiol. 74: 2461-2470. https://doi.org/10.1128/AEM.02272-07
  40. http://www.ncbi.nlm.nih.gov/blast/bl2seq/wblast2.cgi
  41. Borgonie G, Claeys M, Leyns F. 1996. Effect of nematicidal Bacillus thuringiensis strains on free-living nematodes. 2. Ultrastructural analysis of the intoxication process in using time-of-flight mass spectrometry and matrix-free infrared laser desorption and Caenorhabditis elegans. Fundam. Appl. Nematol. 19: 407-414.
  42. Haigh J, Degun A, Eydmann M, Millar M, Wilks M. 2011. Improved performance of bacterium and yeast identification by a commercial matrix-assisted laser desorption ionization-time of flight mass spectrometry system in the clinical microbiology laboratory. J. Clin. Microbiol. 49: 3441. https://doi.org/10.1128/JCM.00576-11
  43. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, et al. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62: 775-806. https://doi.org/10.1128/MMBR.62.3.775-806.1998
  44. Jeyaram K, Romi W, Singh TA, Adewumi GA, Basanti K, Oguntoyinbo FA. 2011. Distinct differentiation of closely related species of bacillus subtilis group with industrial importance. J. Microbiol. Methods. 87: 161-164. https://doi.org/10.1016/j.mimet.2011.08.011
  45. Roh JY, Choi JY, Li MS, Jin BR, Je YH. 2007. Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J. Microbiol. Biotechnol. 17: 547-559.
  46. Chenau J, Fenaille F, Caro V, Haustant M, Diancourt L, Klee SR, et al. 2014. Identification and validation of specific markers of Bacillus anthracis spores by proteomics and genomics approaches. Mol. Cell Proteomics. 13: 716-732. https://doi.org/10.1074/mcp.M113.032946
  47. Lasch P, Beyer W, Nattermann H, Stämmler M, Siegbrecht E, Grunow R, et al. 2009. Identification of Bacillus anthracis by using matrix-assisted laser desorption ionization-time of flight mass spectrometry and artificial neural networks. Appl. Environ. Microbiol. 75: 7229-7242. https://doi.org/10.1128/AEM.00857-09
  48. Lasch P, Wahab T, Weil S, Palyi B, Tomaso H, Zange S, et al. 2015. Identification of highly pathogenic microorganisms by matrix-assisted laser desorption ionization-time of flight mass spectrometry: results of an interlaboratory ring trial. J. Clin. Microbiol. 53: 2632-2640. https://doi.org/10.1128/JCM.00813-15
  49. Ryzhov V, Hathout Y, Fenselau C. 2000. Rapid characterization of spores of Bacillus cereus group bacteria by matrix-assisted laser desorption-ionization time-of-flight mass spectrometry. Appl. Environ. Microbiol. 66: 3828-3834. https://doi.org/10.1128/AEM.66.9.3828-3834.2000
  50. Wilson MK, Abergel RJ, Raymond KN, Arceneaux JE, Byers BR. 2006. Siderophores of Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis. Biochem. Biophys. Res. Commun. 348: 320-325. https://doi.org/10.1016/j.bbrc.2006.07.055
  51. Maughan H, Van der Auwera G. 2011. Bacillus taxonomy in the genomic era finds phenotypes to be essential though often misleading. Infect. Genet. Evol. 11: 789-797. https://doi.org/10.1016/j.meegid.2011.02.001
  52. Fakruddin MD, Sarker N, Ahmed MM, Noor R. 2012. Protein profiling of Bacillus thuringiensis isolated from agroforest soil in Bangladesh. Aspac J. Mol. Biol Biotechnol. 20: 139-145.
  53. Cho SH, Kang SH, Lee YE, Kim SJ, Yoo YB, Bak YS, et al. 2015. Distribution of toxin genes and enterotoxins in Bacillus thuringiensis isolated from microbial insecticide products. J. Microbiol. Biotechnol. 25: 2043-2048. https://doi.org/10.4014/jmb.1506.06025
  54. Modrie P, Beuls E, Mahillon J. 2010. Differential transfer dynamics of pAW63 plasmid among members of the Bacillus cereus group in food microcosms. J. Appl. Microbiol. 108: 888-897. https://doi.org/10.1111/j.1365-2672.2009.04488.x

피인용 문헌

  1. Establishment and Application of Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry for Detection of Shewanella Genus vol.12, 2019, https://doi.org/10.3389/fmicb.2021.625821
  2. Identification and Monitoring of Lactobacillus delbrueckii Subspecies Using Pangenomic-Based Novel Genetic Markers vol.31, pp.2, 2019, https://doi.org/10.4014/jmb.2009.09034
  3. Green nanotechnology for preserving and enriching yogurt with biologically available iron (II) vol.69, 2019, https://doi.org/10.1016/j.ifset.2021.102645
  4. Rapid Detection of Salmonella Enteritidis, Typhimurium, and Thompson by Specific Peak Analysis Using Matrix-Assisted Laser Desorption Ionization Time-of-Flight Mass Spectrometry vol.10, pp.5, 2019, https://doi.org/10.3390/foods10050933
  5. Discrimination of Bacillus cereus Group Members by MALDI-TOF Mass Spectrometry vol.9, pp.6, 2019, https://doi.org/10.3390/microorganisms9061202
  6. Evaluation of B. thuringiensis-based biopesticides in the primary production of fresh produce as a food safety hazard and risk vol.130, 2019, https://doi.org/10.1016/j.foodcont.2021.108390
  7. Development of a high resolution melting method based on a novel molecular target for discrimination between Bacillus cereus and Bacillus thuringiensis vol.151, 2019, https://doi.org/10.1016/j.foodres.2021.110845
  8. Application of MALDI-TOF MS for identification of environmental bacteria: A review vol.305, 2019, https://doi.org/10.1016/j.jenvman.2021.114359