Journal of Microbiology and Biotechnology

  • 제32권2호
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  • Pages.195-204
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  • 2022
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  • 1017-7825(pISSN)
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  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
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Microbiota Analysis and Microbiological Hazard Assessment in Chinese Chive (Allium tuberosum Rottler) Depending on Retail Types

  • Seo, Dong Woo (Department of Food Science and Technology, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Yum, Su-jin (Department of Food Science and Technology, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Lee, Heoun Reoul (Department of Food Science and Technology, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Kim, Seung Min (Department of Food Science and Technology, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Jeong, Hee Gon (Department of Food Science and Technology, College of Agriculture and Life Sciences, Chungnam National University)
  • 투고 : 2021.12.06
  • 심사 : 2021.12.21
  • 발행 : 2022.02.28
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초록

Chinese chive (Allium tuberosum Rottler) has potential risks associated with pathogenic bacterial contamination as it is usually consumed raw. In this study, we investigated the microbiota of Chinese chives purchased from traditional markets and grocery stores in March (Spring) and June (Summer) 2017. Differences in bacterial diversity were observed, and the microbial composition varied across sampling times and sites. In June, potential pathogenic genera, such as Escherichia, Enterobacter, and Pantoea, accounted for a high proportion of the microbiota in samples purchased from the traditional market. A large number of pathogenic bacteria (Acinetobacter lwoffii, Bacillus cereus, Klebsiella pneumoniae, and Serratia marcescens) were detected in the June samples at a relatively high rate. In addition, the influence of the washing treatment on Chinese chive microbiota was analyzed. After storage at 26℃, the washing treatment accelerated the growth of enterohemorrhagic Escherichia coli (EHEC) because it caused dynamic shifts in Chinese chive indigenous microbiota. These results expand our knowledge of the microbiota in Chinese chives and provide data for the prediction and prevention of food-borne illnesses.

키워드

과제정보

This work was supported by the National Research Foundation of Korea funded by the Korean Government (NRF-2019R1F1A1059458), Research Fund and Research Scholarship of Chungnam National University.

참고문헌

  1. Ramesh Mekala KP, Saritha GP, Mohan AD. 2020. Bactericidal effects of Exiguobacterium sp. GM010 pigment against food-borne pathogens. Front. Sust. Food Sys. DOI:10.3389/fsufs.2020.00142.
  2. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. 2015. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med. 12: e1001923. https://doi.org/10.1371/journal.pmed.1001923
  3. Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, FitzGerald M, et al. 2012. Genomic epidemiology of the Escherichia coli O104: H4 outbreaks in Europe, 2011. Proc. Natl. Acad. Sci. USA 109: 3065-3070. https://doi.org/10.1073/pnas.1121491109
  4. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, et al. 2011. Epidemic profile of Shiga-toxin-producing Escherichia coli O104: H4 outbreak in Germany. N. Engl. J. Med. 365: 1771-1780. https://doi.org/10.1056/NEJMoa1106483
  5. Laughlin M, Bottichio L, Weiss J, Higa J, McDonald E, Sowadsky R, et al. 2019. Multistate outbreak of Salmonella Poona infections associated with imported cucumbers, 2015-2016. Epidemiol. Infect. 147: e270. https://doi.org/10.1017/s0950268819001596
  6. Grant J, Wendelboe AM, Wendel A, Jepson B, Torres P, Smelser C, et al. 2008. Spinach-associated Escherichia coli O157: H7 outbreak, Utah and New Mexico, 2006. Emerg. Infect. Dis. 14: 1633. https://doi.org/10.3201/eid1410.071341
  7. Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, et al. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ. Microbiol. 12: 2385-2397. https://doi.org/10.1111/j.1462-2920.2010.02297.x
  8. Lee S, Park A, Yoon H, Lee H, Koo M, Yoon Y. 2014. Comparison of growth and disinfectant resistance of Bacillus cereus isolated from fresh-cut produce and organic vegetables. Food Sci. Biotechnol. 23: 1727-1731. https://doi.org/10.1007/s10068-014-0236-8
  9. Jung Y, Jang H, Matthews KR. 2014. Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb. Biotechnol. 7: 517-527. https://doi.org/10.1111/1751-7915.12178
  10. Ling B, Tang J, Kong F, Mitcham E, Wang S. 2015. Kinetics of food quality changes during thermal processing: a review. Food Bioprocess Technol. 8: 343-358. https://doi.org/10.1007/s11947-014-1398-3
  11. Streit WR, Schmitz RA. 2004. Metagenomics-the key to the uncultured microbes. Curr. Opin. Microbiol. 7: 492-498. https://doi.org/10.1016/j.mib.2004.08.002
  12. Handelsman J. 2004. Metagenomics: application of genomics to uncultured microorganisms. Microb. Mol. Biol. Rev. 68: 669-685. https://doi.org/10.1128/MMBR.68.4.669-685.2004
  13. Bergholz TM, Switt AIM, Wiedmann M. 2014. Omics approaches in food safety: fulfilling the promise? Trends Microbiol. 22: 275-281. https://doi.org/10.1016/j.tim.2014.01.006
  14. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31: 814-821. https://doi.org/10.1038/nbt.2676
  15. Shah N, Tang H, Doak TG, Ye Y. 2011. Comparing bacterial communities inferred from 16S rRNA gene sequencing and shotgun metagenomics, pp. 165-176. Biocomputing 2011, Ed. World Scientific,
  16. Yu Y-C, Yum S-J, Jeon D-Y, Jeong H-G. 2018. Analysis of the microbiota on lettuce (Lactuca sativa L.) cultivated in South Korea to identify foodborne pathogens. J. Microbiol. Biotechnol. 28: 1318-1331. https://doi.org/10.4014/jmb.1803.03007
  17. Jeon D-y, Yum S-j, Seo DW, Kim SM, Jeong HG. 2019. Leaf-associated microbiota on perilla (Perilla frutescens var. frutescens) cultivated in South Korea to detect the potential risk of food poisoning. Food Res. Int. 126: 108664. https://doi.org/10.1016/j.foodres.2019.108664
  18. Yabuki Y, Mukaida Y, Saito Y, Oshima K, Takahashi T, Muroi E, et al. 2010. Characterisation of volatile sulphur-containing compounds generated in crushed leaves of Chinese chive (Allium tuberosum Rottler). Food Chem.120: 343-348. https://doi.org/10.1016/j.foodchem.2009.11.028
  19. Imahori Y, Suzuki Y, Uemura K, Kishioka I, Fujiwara H, Ueda Y, et al. 2004. Physiological and quality responses of Chinese chive leaves to low oxygen atmosphere. Postharvest Biol. Technol. 31: 295-303. https://doi.org/10.1016/j.postharvbio.2003.09.004
  20. Worsfold D, Worsfold PM, Griffith CJ. 2004. An assessment of food hygiene and safety at farmers' markets. Int. J. Environ. Health Res. 14: 109-119. https://doi.org/10.1080/0960312042000209507
  21. Scheinberg JA, Dudley EG, Campbell J, Roberts B, DiMarzio M, DebRoy C, et al. 2017. Prevalence and phylogenetic characterization of Escherichia coli and hygiene indicator bacteria isolated from leafy green produce, beef, and pork obtained from farmers' markets in Pennsylvania. J. Food Prot. 80: 237-244. https://doi.org/10.4315/0362-028X.JFP-16-282
  22. Kim H-E, Lee J-J, Lee M-J, Kim B-S. 2019. Analysis of microbiome in raw chicken meat from butcher shops and packaged products in South Korea to detect the potential risk of foodborne illness. Food Res. Int. 122: 517-527. https://doi.org/10.1016/j.foodres.2019.05.032
  23. Hanshew AS, Mason CJ, Raffa KF, Currie CR. 2013. Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J. Microbiol. Methods 95: 149-155. https://doi.org/10.1016/j.mimet.2013.08.007
  24. Kumar PS, Brooker MR, Dowd SE, Camerlengo T. 2011. Target region selection is a critical determinant of community fingerprints generated by 16S pyrosequencing. PLoS One 6: e20956. https://doi.org/10.1371/journal.pone.0020956
  25. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200. https://doi.org/10.1093/bioinformatics/btr381
  26. Williams TR, Moyne A-L, Harris LJ, Marco ML. 2013. Season, irrigation, leaf age, and Escherichia coli inoculation influence the bacterial diversity in the lettuce phyllosphere. PLoS One 8: e68642. https://doi.org/10.1371/journal.pone.0068642
  27. Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, Leveau JH. 2012. Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J. 6: 1812-1822. https://doi.org/10.1038/ismej.2012.32
  28. Ingraham J. 1958. Growth of psychrophilic bacteria. J. Bacteriol. 76: 75. https://doi.org/10.1128/jb.76.1.75-80.1958
  29. Turner TR, James EK, Poole PS. 2013. The plant microbiome. Genome Biol. 14: 209. https://doi.org/10.1186/gb-2013-14-6-209
  30. Kim D, Hong S, Kim Y-T, Ryu S, Kim HB, Lee J-H. 2018. Metagenomic approach to identifying foodborne pathogens on Chinese cabbage. J. Microbiol. Biotechnol. 28: 227-235. https://doi.org/10.4014/jmb.1710.10021
  31. Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A. 2011. Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb. Ecol. 62: 188-197. https://doi.org/10.1007/s00248-011-9883-y
  32. Sanders W, Sanders CC. 1997. Enterobacter spp.: pathogens poised to flourish at the turn of the century. Clin. Microbiol. Rev. 10: 220-241. https://doi.org/10.1128/cmr.10.2.220
  33. Abbas Z, Authman S, Al-Ezee A. 2017. Temperature effects on growth of the biocontrol agent Pantoea agglomerans (an oval isolate from Iraqi soils). J. Adv. Lab. Res. Biol. 8: 85-88.
  34. Jung I, Park D-H, Park K. 2002. A study of the growth condition and solubilization of phosphate from hydroxyapatite by Pantoea agglomerans. Biotechnol. Bioprocess Eng. 7: 201-205. https://doi.org/10.1007/BF02932970
  35. Fonseca P, Moreno R, Rojo F. 2011. Growth of Pseudomonas putida at low temperature: global transcriptomic and proteomic analyses. Environ. Microbiol. Rep. 3: 329-339. https://doi.org/10.1111/j.1758-2229.2010.00229.x
  36. Yabuuchi E, Wang L, Arakawa M, Yano I. 1993. Survival of Pseudomonas pseudomallei strains at 5 degrees C. Kansenshogaku Zasshi 67: 331-335. https://doi.org/10.11150/kansenshogakuzasshi1970.67.331
  37. Stover CK, Pham XQ, Erwin A, Mizoguchi S, Warrener P, Hickey M, et al. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964. https://doi.org/10.1038/35023079
  38. Bazhanov DP, Yang K, Li H, Li C, Li J, Chen X, et al. 2017. Colonization of plant roots and enhanced atrazine degradation by a strain of Arthrobacter ureafaciens. Appl. Microbiol. Biotechnol. 101: 6809-6820. https://doi.org/10.1007/s00253-017-8405-3
  39. Safdarian M, Askari H, Shariati V, Nematzadeh G. 2019. Transcriptional responses of wheat roots inoculated with Arthrobacter nitroguajacolicus to salt stress. Sci. Rep. 9: 1-12. https://doi.org/10.1038/s41598-018-37186-2
  40. Singh RN, Gaba S, Yadav AN, Gaur P, Gulati S, Kaushik R, et al. 2016. First high quality draft genome sequence of a plant growth promoting and cold active enzyme producing psychrotrophic Arthrobacter agilis strain L77. Stand. Genomic. Sci. 11: 54. https://doi.org/10.1186/s40793-016-0176-4
  41. Sajjad W, Din G, Rafiq M, Iqbal A, Khan S, Zada S, et al. 2020. Pigment production by cold-adapted bacteria and fungi: colorful tale of cryosphere with wide range applications. Extremophiles 24: 447-473. https://doi.org/10.1007/s00792-020-01180-2
  42. Cruz AT, Cazacu AC, Allen CH. 2007. Pantoea agglomerans, a plant pathogen causing human disease. J. Clin. Microbiol. 45: 1989-1992. https://doi.org/10.1128/JCM.00632-07
  43. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140. https://doi.org/10.1038/nrmicro818
  44. Ofek M, Hadar Y, Minz D. 2012. Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS One 7: e40117. https://doi.org/10.1371/journal.pone.0040117
  45. Kim DY, Kim J, Lee YM, Lee JS, Shin D-H, Ku B-H, et al. 2021. Identification and Characterization of a novel, cold-adapted d-Xylobiose-and d-Xylose-releasing endo-β-1, 4-xylanase from an antarctic soil bacterium, Duganella sp. PAMC 27433. Biomolecules 11: 680. https://doi.org/10.3390/biom11050680
  46. Gobbetti M, Rizzello C. 2014. Arthrobacter. Encyclopedia of Food Microbiol. 69-87.
  47. Mena KD, Gerba CP. 2009. Risk assessment of Pseudomonas aeruginosa in water. Rev. Environ. Contam. Toxicol. 201: 71-115. https://doi.org/10.1007/978-1-4419-0032-6_3
  48. Grimont F, Grimont PA. 2015. Serratia. Bergey's manual of systematics of archaea and bacteria. pp. 1-22.
  49. Kim SJ, Shin SC, Hong SG, Lee YM, Lee H, Lee J, et al. 2012. Genome sequence of Janthinobacterium sp. strain PAMC 25724, isolated from alpine glacier cryoconit. Am. Soc. Microbiol. 194: 2096.
  50. Chen F, Guo Y, Wang J, Li J, Wang H. 2007. Biological control of grape crown gall by Rahnella aquatilis HX2. Plant Dis. 91: 957-963. https://doi.org/10.1094/pdis-91-8-0957
  51. Kot W, Neve H, Heller KJ, Vogensen FK. 2014. Bacteriophages of Leuconostoc, Oenococcus, and Weissella. Front. Microbiol. 5: 186. https://doi.org/10.3389/fmicb.2014.00186
  52. Regalado NG, Martin G, Antony SJ. 2009. Acinetobacter lwoffii: bacteremia associated with acute gastroenteritis. Travel Med. Infect. Dis. 7: 316-317. https://doi.org/10.1016/j.tmaid.2009.06.001
  53. Kotiranta A, Lounatmaa K, Haapasalo M. 2000. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect. 2: 189-198. https://doi.org/10.1016/S1286-4579(00)00269-0
  54. Struve C, Krogfelt KA. 2004. Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ. Microbiol. 6: 584-590. https://doi.org/10.1111/j.1462-2920.2004.00590.x
  55. Davies Y, Cunha M, Oliveira M, Oliveira M, Philadelpho N, Romero D, et al. 2016. Virulence and antimicrobial resistance of Klebsiella pneumoniae isolated from passerine and psittacine birds. Avian Pathol. 45: 194-201. https://doi.org/10.1080/03079457.2016.1142066
  56. Oogai Y, Matsuo M, Hashimoto M, Kato F, Sugai M, Komatsuzawa H. 2011. Expression of virulence factors by Staphylococcus aureus grown in serum. Appl. Environ. Microbiol. 77: 8097-8105. https://doi.org/10.1128/AEM.05316-11
  57. Bell C. 2002. Approach to the control of entero-haemorrhagic Escherichia coli (EHEC). Int. J. Food Microbiol. 78: 197-216. https://doi.org/10.1016/S0168-1605(02)00188-5
  58. Viazis S, Akhtar M, Feirtag J, Diez-Gonzalez F. 2011. Reduction of Escherichia coli O157: H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiol. 28: 149-157. https://doi.org/10.1016/j.fm.2010.09.009
  59. Koseki S, Itoh K. 2001. Prediction of microbial growth in fresh-cut vegetables treated with acidic electrolyzed water during storage under various temperature conditions. J. Food Prot. 64: 1935-1942. https://doi.org/10.4315/0362-028X-64.12.1935