Investigating the responses of Cronobacter sakazakii to garlic-drived organosulfur compounds: A systematic study of pathogenic-bacterium injury by use of high-throughput whole-transcriptome sequencing and confocal micro-raman spectroscopy

Applied and Environmental Microbiology

Volumn 80, Issue 3, 2014, Pages 959-971

  Feng, Shaolong ^a,b   Eucker, Tyson P ^c   Holly, Mayumi K ^c   Konkel, Michael E ^c   Lu, Xiaonan ^b   Wang, Shuo ^a  

^a TIANJIN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL COMPOUNDS; ANTIMICROBIAL MECHANISMS; BAYESIAN PROBABILITIES; GENE EXPRESSION PATTERNS; INTERVENTION STRATEGY; MORPHOLOGICAL VARIATION; ORGANOSULFUR COMPOUNDS; SECONDARY STRUCTURES;

AMINO ACIDS; BACTERIA; BACTERIOLOGY; CELLS; CYTOLOGY; GENE EXPRESSION; PRINCIPAL COMPONENT ANALYSIS; RAMAN SPECTROSCOPY; RNA; SCANNING ELECTRON MICROSCOPY;

SULFUR COMPOUNDS;

ANTIMICROBIAL ACTIVITY; BACTERIUM; BAYESIAN ANALYSIS; ENZYME ACTIVITY; FOOD PRODUCTION; INFECTIVITY; INJURY; MENINGITIS; ORGANIC SULFUR COMPOUND; PATHOGEN; PROTEIN; RAMAN SPECTROSCOPY; RISK FACTOR;

AJOENE; ALLYL COMPOUND; ALLYL SULFIDE; ANTIINFECTIVE AGENT; DISULFIDE; SULFIDE; TRANSCRIPTOME;

ARTICLE; CHEMISTRY; CRONOBACTER SAKAZAKII; DRUG EFFECT; GARLIC; ISOLATION AND PURIFICATION; PROTEIN CONFORMATION; RAMAN SPECTROMETRY; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALLYL COMPOUNDS; ANTI-BACTERIAL AGENTS; CRONOBACTER SAKAZAKII; DISULFIDES; GARLIC; MICROSCOPY, ELECTRON, SCANNING; PROTEIN CONFORMATION; SPECTRUM ANALYSIS, RAMAN; SULFIDES; TRANSCRIPTOME;

EID: 84892970887     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03460-13     Document Type: Article

References (67)

1. Zhou X, Fu S, Gao J, Chen H. 2011. Enterobacter sakazakii: an emerging foodborne pathogenic bacterium. Ann. Microbiol. 62:1-5.
2. Amalaradjou MA, Hoagland TA, Venkitanarayanan K. 2009. Inactivation of Enterobacter sakazakii in reconstituted infant formula by transcinnamaldehyde. Int. J. Food Microbiol. 129:146-149. http://dx.doi.org /10.1016/j.ijfoodmicro.2008.11.016.
3. Amalaradjou MA, Venkitanarayanan K. 2011. Effect of transcinnamaldehyde on inhibition and inactivation of Cronobacter sakazakii biofilm on abiotic surfaces. J. Food Prot. 74:200-208. http://dx.doi.org/10 .4315/0362-028X.JFP-10-296.
4. Chenu JW, Cox JM. 2009. Cronobacter ('Enterobacter sakazakii'): current status and future prospects. Lett. Appl. Microbiol. 49:153-159. http://dx .doi.org/10.1111/j.1472-765X.2009.02651.x.
5. Kim H, Ryu JH, Beuchat LR. 2007. Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm. Appl. Environ. Microbiol. 73:1256-1265. http: //dx.doi.org/10.1128/AEM.01766-06.
6. Friedemann M. 2009. Epidemiology of invasive neonatal Cronobacter (Enterobacter sakazakii) infections. Eur. J. Clin. Microbiol. Infect. Dis. 28:1297-1304. http://dx.doi.org/10.1007/s10096-009-0779-4.
7. Bowen AB, Braden CR. 2006. Invasive Enterobacter sakazakii disease in infants. Emerging Infect. Dis. 12:1185-1189.
8. Forsythe SJ. 2005. Enterobacter sakazakii and other bacteria in powdered infant milk formula. Matern. Child Nutr. 1:44-50. http://dx.doi.org/10 .1111/j.1740-8709.2004.00008.x.
9. Friedman M, Henika PR, Mandrell RE. 2003. Antibacterial activities of phenolic benzaldehydes and benzoic acids against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. J. Food Prot. 66:1811-1821.
10. De R, Kundu P, Swarnakar S, Ramamurthy T, Chowdhury A, Nair GB, Mukhopadhyay AK. 2009. Antimicrobial activity of curcumin against Helicobacter pylori isolates from India and during infections in mice. Antimicrob. Agents Chemother. 53:1592-1597. http://dx.doi.org/10.1128 /AAC.01242-08.
11. Lacombe A, Wu VC, Tyler S, Edwards K. 2010. Antimicrobial action of the American cranberry constituents; phenolics, anthocyanins, and organic acids, against Escherichia coli O157: H7. Int. J. Food Microbiol. 139: 102-107. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.01.035.
12. Wright GD, Sutherland AD. 2007. New strategies for combating multidrug-resistant bacteria. Trends Mol. Med. 13:260-267. http://dx.doi.org /10.1016/j.molmed.2007.04.004.
13. Erkoç Ş , Sümer S, Erkoç F. 2003. Structural and electronic properties of ajoene molecule. J. Mol. Struct. (Theochem.) 631:271-276. http://dx.doi .org/10.1016/S0166-1280(03)00259-8.
14. Lee DY, Li H, Lim HJ, Lee HJ, Jeon R, Ryu JH. 2012. Anti-inflammatory activity of sulfur-containing compounds from garlic. J. Med. Food 15: 992-999. http://dx.doi.org/10.1089/jmf.2012.2275.
15. Corzomartinez M, Corzo N, Villamiel M. 2007. Biological properties of onions and garlic. Trends Food Sci. Technol. 18:609-625. http://dx.doi .org/10.1016/j.tifs.2007.07.011.
16. Ilic D, Nikolic V, Nikolic L, Stankovic M, Stanojevic L, Cakic M. 2011. Allicin and related compounds: Biosynthesis, synthesis and pharmacological activity. F.U. Phys. Chem. Technol. 9:9-20. http://dx.doi.org/10.2298 /FUPCT1101009I.
17. Kim YS, Kim KS, Han I, Kim MH, Jung MH, Park HK. 2012. Quantitative and qualitative analysis of the antifungal activity of allicin alone and in combination with antifungal drugs. PLoS One 7:e38242. http://dx.doi .org/10.1371/journal.pone.0038242.
18. Lu X, Samuelson DR, Rasco BA, Konkel ME. 2012. Antimicrobial effect of diallyl sulphide on Campylobacter jejuni biofilms. J. Antimicrob. Chemother. 67:1915-1926. http://dx.doi.org/10.1093/jac/dks138.
19. Ohta R, Yamada N, Kaneko H, Ishikawa K, Fukuda H, Fujino T, Suzuki A. 1999. In vitro inhibition of the growth of Helicobacter pylori by oilmacerated garlic constituents. Antimicrob. Agents Chemother. 43:1811-1812.
20. Block E, Ahmad S, Catalfamo JL, Jain MK, Apitz-Castro R. 1986. The chemistry of alkyl thiosulfinate esters. 9. Antithrombotic organosulfur compounds from garlic: structural, mechanistic, and synthetic studies. J. Am. Chem. Soc. 108:7045-7055. http://dx.doi.org/10.1021/ja00282a033.
21. Ishikawa K, Naganawa R, Yoshida H, Iwata N, Fukuda H, Fujino T, Suzuki A. 1996. Antimutagenic effects of ajoene, an organosulfur compound derived from garlic. Biosci. Biotechnol. Biochem. 60:2086-2088. http://dx.doi.org/10.1271/bbb.60.2086.
22. Yoshida H, Iwata N, Katsuzaki H, Naganawa R, Ishikawa K, Fukuda H, Fujino T, Suzuki A. 1998. Antimicrobial activity of a compound isolated from an oil-macerated garlic extract. Biosci. Biotechnol. Biochem. 62: 1014-1017. http://dx.doi.org/10.1271/bbb.62.1014.
23. Velliyagounder K, Ganeshnarayan K, Velusamy SK, Fine DH. 2012. In vitro efficacy of diallyl sulfides against the periodontopathogen Aggregatibacter actinomycetemcomitans. Antimicrob. Agents Chemother. 56:2397-2407. http://dx.doi.org/10.1128/AAC.00020-12.
24. Lu X, Rasco BA, Jabal JM, Aston DE, Lin M, Konkel ME. 2011. Investigating antibacterial effects of garlic (Allium sativum) concentrate and garlic-derived organosulfur compounds on Campylobacter jejuni by using Fourier transform infrared spectroscopy, Raman spectroscopy, and electron microscopy. Appl. Environ. Microbiol. 77:5257-5269. http://dx .doi.org/10.1128/AEM.02845-10.
25. Jakobsen TH, van Gennip M, Phipps RK, Shanmugham MS, Christensen LD, Alhede M, Skindersoe ME, Rasmussen TB, Friedrich K, Uthe F, Jensen PO, Moser C, Nielsen KF, Eberl L, Larsen TO, Tanner D, Hoiby N, Bjarnsholt T, Givskov M. 2012. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob. Agents Chemother. 56:2314-2325. http://dx.doi.org/10.1128 /AAC.05919-11.
26. Naganawa R, Iwata N, Ishikawa K, Fukuda H, Fujino T, Suzuki A. 1996. Inhibition of microbial growth by ajoene, a sulfur-containing compound derived from garlic. Appl. Environ. Microbiol. 62:4238-4242.
27. Cady NC, McKean KA, Behnke J, Kubec R, Mosier AP, Kasper SH, Burz DS, Musah RA. 2012. Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS One 7:e38492. http://dx.doi.org/10.1371 /journal.pone.0038492.
28. Kyung KH. 2012. Antimicrobial properties of Allium species. Curr. Opin. Biotechnol. 23:142-147. http://dx.doi.org/10.1016/j.copbio.2011.08.004.
29. San-Blas G, San-Blas F, Gil F, Marino L, Apitz-Castro R. 1989. Inhibition of growth of the dimorphic fungus Paracoccidioides brasiliensis by ajoene. Antimicrob. Agents Chemother. 33:1641-1644. http://dx.doi.org /10.1128/AAC.33.9.1641.
30. Yoshida S, Kasuga S, Hayashi N, Ushiroguchi T, Matsuura H, Nakagawa S. 1987. Antifungal activity of ajoene derived from garlic. Appl. Environ. Microbiol. 53:615-617.
31. Lu X, Rasco BA, Kang DH, Jabal JM, Aston DE, Konkel ME. 2011. Infrared and Raman spectroscopic studies of the antimicrobial effects of garlic concentrates and diallyl constituents on foodborne pathogens. Anal. Chem. 83:4137-4146. http://dx.doi.org/10.1021/ac2001498.
32. Yoshida H, Katsuzaki H, Ohta R, Ishikawa K, Fukuda H, Fujino T, Suzuki A. 1999. An organosulfur compound isolated from oil-macerated garlic extract, and its antimicrobial effect. Biosci. Biotechnol. Biochem. 63:588-590. http://dx.doi.org/10.1271/bbb.63.588.
33. Lu X, Al-Qadiri HM, Lin M, Rasco BA. 2011. Application of midinfrared and Raman spectroscopy to the study of bacteria. Food Bioprocess Technol. 4:919-935. http://dx.doi.org/10.1007/s11947-011-0516-8.
34. Palchaudhuri S, Rehse SJ, Hamasha K, Syed T, Kurtovic E, Kurtovic E, Stenger J. 2011. Raman spectroscopy of xylitol uptake and metabolism in Gram-positive and Gram-negative bacteria. Appl. Environ. Microbiol. 77: 131-137. http://dx.doi.org/10.1128/AEM.01458-10.
35. Lu X, Liu Q, Wu D, Al-Qadiri HM, Al-Alami NI, Kang DH, Shin JH, Tang J, Jabal JM, Aston ED, Rasco BA. 2011. Using of infrared spectroscopy to study the survival and injury of Escherichia coli O157:H7, Campylobacter jejuni and Pseudomonas aeruginosa under cold stress in low nutrient media. Food Microbiol. 28:537-546. http://dx.doi.org/10.1016/j.fm.2010.11 .002.
36. Lu X, Weakley AT, Aston DE, Rasco BA, Wang S, Konkel ME. 2012. Examination of nanoparticle inactivation of Campylobacter jejuni biofilms using infrared and Raman spectroscopies. J. Appl. Microbiol. 113:952-963. http://dx.doi.org/10.1111/j.1365-2672.2012.05373.x.
37. Wang S, Deng K, Zaremba S, Deng X, Lin C, Wang Q, Tortorello ML, Zhang W. 2009. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl. Environ. Microbiol. 75:6110-6123. http://dx.doi .org/10.1128/AEM.00914-09.
38. Wang S, Phillippy AM, Deng K, Rui X, Li Z, Tortorello ML, Zhang W. 2010. Transcriptomic responses of Salmonella enterica serovars Enteritidis and Typhimurium to chlorine-based oxidative stress. Appl. Environ. Microbiol. 76:5013-5024. http://dx.doi.org/10.1128/AEM.00823-10.
39. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G. 2001. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183:4562-4570. http://dx.doi.org/10.1128/JB.183.15.4562-4570.2001.
40. Deng X, Li Z, Zhang W. 2012. Transcriptome sequencing of Salmonella enterica serovar Enteritidis under desiccation and starvation stress in peanut oil. Food Microbiol. 30:311-315. http://dx.doi.org/10.1016/j.fm.2011 .11.001.
41. Croucher NJ, Thomson NR. 2010. Studying bacterial transcriptomes using RNA-seq. Curr. Opin. Microbiol. 13:619-624. http://dx.doi.org/10 .1016/j.mib.2010.09.009.
42. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, Yu L, Assefa SA, He M, Croucher NJ, Pickard DJ. 2009. A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genet. 5:e1000569. http://dx.doi.org/10.1371/journal.pgen .1000569.
43. Giannoukos G, Ciulla DM, Huang K, Haas BJ, Izard J, Levin JZ, Livny J, Earl AM, Gevers D, Ward DV. 2012. Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol. 13:R23. http://dx.doi.org/10.1186/gb-2012-13-3-r23.
44. Mandlik A, Livny J, Robins WP, Ritchie JM, Mekalanos JJ, Waldor MK. 2011. RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10:165-174. http://dx.doi.org /10.1016/j.chom.2011.07.007.
45. Lieber CA, Mahadevan-Jansen A. 2003. Automated method for subtraction of fluorescence from biological Raman spectra. Appl. Spectrosc. 57: 1363-1367. http://dx.doi.org/10.1366/000370203322554518.
46. Weakley AT, Griffiths PR, Aston DE. 2012. Automatic baseline subtraction of vibrational spectra using minima identification and discrimination via adaptive, least-squares thresholding. Appl. Spectrosc. 66:519-529. http://dx.doi.org/10.1366/110-06526.
47. Bocklitz T, Walter A, Hartmann K, Rosch P, Popp J. 2011. How to pre-process Raman spectra for reliable and stable models? Anal. Chim. Acta 704:47-56. http://dx.doi.org/10.1016/j.aca.2011.06.043.
48. Lu X, Huang Q, Miller WG, Aston DE, Xu J, Xue F, Zhang H, Rasco BA, Wang S, Konkel ME. 2012. Comprehensive detection and discrimination of Campylobacter species by use of confocal micro-Raman spectroscopy and multilocus sequence typing. J. Clin. Microbiol. 50:2932-2946. http://dx.doi.org/10.1128/JCM.01144-12.
49. Lu X, Samuelson DR, Xu Y, Zhang H, Wang S, Rasco BA, Xu J, Konkel ME. 2013. Detecting and tracking nosocomial methicillin-resistant Staphylococcus aureus using a microfluidic SERS biosensor. Anal. Chem. 85: 2320-2327. http://dx.doi.org/10.1021/ac303279u.
50. Rösch P, Harz M, Schmitt M, Peschke KD, Ronneberger O, Burkhardt H, Motzkus HW, Lankers M, Hofer S, Thiele H, Popp J. 2005. Chemotaxonomic identification of single bacteria by micro-Raman spectroscopy: application to clean-room-relevant biological contaminations. Appl. Environ. Microbiol. 71:1626-1637. http://dx.doi.org/10.1128/AEM .71.3.1626-1637.2005.
51. Lu X, Webb M, Talbott M, Van Eenennaam J, Palumbo A, Linares-Casenave J, Doroshov S, Struffenegger P, Rasco B. 2010. Distinguishing ovarian maturity of farmed white sturgeon (Acipenser transmontanus) by Fourier transform infrared spectroscopy: a potential tool for caviar production management. J. Agric. Food Chem. 58:4056-4064. http://dx.doi .org/10.1021/jf9038502.
52. Morrey JR. 1968. On determining spectral peak positions from composite spectra with a digital computer. Anal. Chem. 40:905-914. http://dx.doi .org/10.1021/ac60262a006.
53. Hamel L, Brown CW. 2012. Bayesian probability approach to feature significance for infrared spectra of bacteria. Appl. Spectrosc. 66:48-59.
54. Correa E, Goodacre R. 2011. A genetic algorithm-Bayesian network approach for the analysis of metabolomics and spectroscopic data: application to the rapid detection of Bacillus spores and identification of Bacillus species. BMC Bioinformatics 12:33. http://dx.doi.org/10.1186/1471-2105 -12-33.
55. Lu X, Liu Q, Benavides-Montano JA, Nicola AV, Aston DE, Rasco BA, Aguilar HC. 2013. Detection of receptor-induced glycoprotein conformational changes on enveloped virions using confocal micro-Raman spectroscopy. J. Virol. 87:3130-3142. http://dx.doi.org/10.1128/JVI.03220-12.
56. Feldberg R, Chang S, Kotik A, Nadler M, Neuwirth Z, Sundstrom D, Thompson N. 1988. In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Chemother. 32:1763-1768. http: //dx.doi.org/10.1128/AAC.32.12.1763.
57. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4:44-57. http://dx.doi.org/10.1038/nprot.2008.211.
58. Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623-633. http://dx.doi.org/10.1038/nrmicro2415.
59. Naumann D. 2001. FT-infrared and FT-Raman spectroscopy in biomedical research. Appl. Spectrosc. Rev. 36:239-298. http://dx.doi.org/10.1081 /ASR-100106157.
60. Movasaghi Z, Rehman S, Rehman IU. 2007. Raman spectroscopy of biological tissues. Appl. Spectrosc. Rev. 42:493-541. http://dx.doi.org/10 .1080/05704920701551530.
61. Kyung K, Lee Y. 2001. Antimicrobial activities of sulfur compounds derived from S-alk (en) yl-L-cysteine sulfoxides in Allium and Brassica. Food Rev. Int. 17:183-198. http://dx.doi.org/10.1081/FRI-100000268.
62. Ross Z, O'Gara EA, Hill DJ, Sleightholme H, Maslin DJ. 2001. Antimicrobial properties of garlic oil against human enteric bacteria: evaluation of methodologies and comparisons with garlic oil sulfides and garlic powder. Appl. Environ. Microbiol. 67:475-480. http://dx.doi.org/10.1128 /AEM.67.1.475-480.2001.
63. O'Gara EA, Hill DJ, Maslin DJ. 2000. Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Appl. Environ. Microbiol. 66:2269-2273. http://dx.doi.org/10.1128/AEM.66.5.2269-2273 .2000.
64. Kaschula CH, Hunter R, Parker MI. 2010. Garlic-derived anticancer agents: structure and biological activity of ajoene. Biofactors 36: 78 -85.
65. Cavallito CJ, Buck JS, Suter C. 1944. Allicin, the antibacterial principle of Allium sativum. II. Determination of the chemical structure. J. Am. Chem. Soc. 66:1952-1954.
66. Miron T, Rabinkov A, Mirelman D, Wilchek M, Weiner L. 2000. The mode of action of allicin: its ready permeability through phospholipid membranes may contribute to its biological activity. Biochim. Biophys. Acta 1463:20-30. http://dx.doi.org/10.1016/S0005-2736(99)00174-1.
67. Moen B, Oust A, Langsrud ø, Dorrell N, Marsden GL, Hinds J, Kohler A, Wren BW, Rudi K. 2005. Explorative multifactor approach for investigating global survival mechanisms of Campylobacter jejuni under environmental conditions. Appl. Environ. Microbiol. 71:2086-2094. http://dx .doi.org/10.1128/AEM.71.4.2086-2094.2005.