Fresh fruits and vegetables can harbor large and diverse populations of bacteria. However, most of the work on produce-associated bacteria has focused on a relatively small number of pathogenic bacteria and, as a result, we know far less about the overall diversity and composition of those bacterial communities found on produce and how the structure of these communities varies across produce types. Moreover, we lack a comprehensive view of the potential effects of differing farming practices on the bacterial communities to which consumers are exposed. We addressed these knowledge gaps by assessing bacterial community structure on conventional and organic analogs of eleven store-bought produce types using a culture-independent approach, 16 S rRNA gene pyrosequencing. Our results demonstrated that the fruits and vegetables harbored diverse bacterial communities, and the communities on each produce type were significantly distinct from one another. However, certain produce types (i.e., sprouts, spinach, lettuce, tomatoes, peppers, and strawberries) tended to share more similar communities as they all had high relative abundances of taxa belonging to the family Enterobacteriaceae when compared to the other produce types (i.e., apples, peaches, grapes, and mushrooms) which were dominated by taxa belonging to the Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria phyla. Although potentially driven by factors other than farming practice, we also observed significant differences in community composition between conventional and organic analogs within produce types. These differences were often attributable to distinctions in the relative abundances of Enterobacteriaceae taxa, which were generally less abundant in organically-grown produce. Taken together, our results suggest that humans are exposed to substantially different bacteria depending on the types of fresh produce they consume with differences between conventionally and organically farmed varieties contributing to this variation.
References
[1]
King AD, Magnuson JA, T？r？k T, Goodman N (1991) Microbial flora and storage quality of partially processed lettuce. J Food Sci 56: 459–461.
[2]
Badosa E, Trias R, Parés D, Pla M, Montesinos E, et al. (2008) Microbiological quality of fresh fruit and vegetable products in Catalonia (Spain) using normalised plate-counting methods and real time polymerase chain reaction (QPCR). J Sci Food Agric 88: 605–611.
[3]
Ponce AG, Agüero MV, Roura SI, del Valle CE, Moreira MR (2008) Dynamics of Indigenous Microbial Populations of Butter Head Lettuce Grown in Mulch and on Bare Soil. J Food Sci 73: M257–M263.
[4]
Oliveira M, Usall J, Vi？as I, Anguera M, Gatius F, et al. (2010) Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol 27: 679–684.
[5]
Rastogi G, Sbodio A, Tech JJ, Suslow TV, Coaker GL, et al.. (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J: 1–11.
[6]
Nguyen-the C, Carlin F (1994) The microbiology of minimally processed fresh fruits and vegetables. Crit Rev Food Sci Nutr 34: 371–401.
[7]
Liao CH, Fett WF (2001) Analysis of native microflora and selection of strains antagonistic to human pathogens on fresh produce. J Food Prot 64: 1110–1115.
[8]
Beuchat LR (1996) Pathogenic microorganisms associated with fresh produce. J Food Prot 59: 204–216.
[9]
Critzer FJ, Doyle MP (2010) Microbial ecology of foodborne pathogens associated with produce. Curr Opin Biotechnol 21: 125–130.
[10]
Harris LJ, Farber JN, Beuchat LR, Parish ME, Suslow TV, et al. (2003) Outbreaks associated with fresh produce: Incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Compr Rev Food Sci F 2: 78–141.
[11]
Fatica MK, Schneider KR (2011) Salmonella and produce: Survival in the plant environment and implications in food safety. Virulence 2: 573–579.
[12]
Hanski I, von Hertzen L, Fyhrquist N, Koskinen K, Torppa K, et al. (2012) Environmental biodiversity, human microbiota, and allergy are interrelated. Proc Natl Acad Sci U S A 109: 8334–8339.
[13]
Gram L, Ravn L, Rasch M, Bruhn JB, Christensen AB, et al. (2002) Food spoilage–interactions between food spoilage bacteria. Int J Food Microbiol 78: 79–97.
[14]
Flores GE, Bates ST, Caporaso JG, Lauber CL, Leff JW, et al.. (2012) Diversity, distribution and sources of bacteria in residential kitchens. Environ Microbiol In press.
[15]
Rudi K, Flateland SL, Hanssen JF, Bengtsson G, Nissen H (2002) Development and evaluation of a 16 S ribosomal dna array-based approach for describing complex microbial communities in ready-to-eat vegetable salads packed in a modified atmosphere. Appl Environ Microbiol 68: 1146–1156.
[16]
Lopez-Velasco G, Welbaum GE, Boyer RR, Mane SP, Ponder MA (2011) Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16 S rRNA amplicons. J Appl Microbiol 110: 1203–1214.
[17]
Granado J, Thürig B, Kieffer E, Petrini L, Fliessbach A, et al. (2008) Culturable fungi of stored “golden delicious” apple fruits: a one-season comparison study of organic and integrated production systems in Switzerland. Microb Ecol 56: 720–732.
[18]
Ottesen AR, White JR, Skaltsas DN, Newell MJ, Walsh CS (2009) Impact of organic and conventional management on the phyllosphere microbial ecology of an apple crop. J Food Prot 72: 2321–2325.
[19]
Enya J, Shinohara H, Yoshida S, Tsukiboshi T, Negishi H, et al. (2007) Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microb Ecol 53: 524–536.
[20]
Shi X, Wu Z, Namvar a, Kostrzynska M, Dunfield K, et al. (2009) Microbial population profiles of the microflora associated with pre- and postharvest tomatoes contaminated with Salmonella typhimurium or Salmonella montevideo. J Appl Microbiol 107: 329–338.
[21]
Teplitski M, Warriner K, Bartz J, Schneider KR (2011) Untangling metabolic and communication networks: interactions of enterics with phytobacteria and their implications in produce safety. Trends Microbiol 19: 121–127.
[22]
Kim M, Singh D, Lai-Hoe A, Go R, Abdul Rahim R, et al. (2012) Distinctive phyllosphere bacterial communities in tropical trees. Microb Ecol 63: 674–681.
[23]
Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria. Environ Microbiol 12: 2885–2893.
[24]
Kroupitski Y, Pinto R, Belausov E, Sela S (2011) Distribution of Salmonella typhimurium in romaine lettuce leaves. Food Microbiol 28: 990–997.
[25]
Zagory D (1999) Effects of post-processing handling and packaging on microbial populations. Postharvest Biol Technol 15: 313–321.
[26]
Schmid F, Moser G, Müller H, Berg G (2011) Functional and structural microbial diversity in organic and conventional viticulture: organic farming benefits natural biocontrol agents. Appl Environ Microbiol 77: 2188–2191.
[27]
Yashiro E, Spear RN, McManus PS (2011) Culture-dependent and culture-independent assessment of bacteria in the apple phyllosphere. J Appl Microbiol 110: 1284–1296.
[28]
Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105: 17994–17999.
[29]
Chelius MK, Triplett EW (2001) The diversity of Archaea and Bacteria in association with the roots of Zea mays L. Microb Ecol. 41: 252–263.
[30]
Caporaso J, Kuczynski J, Stombaugh J (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
[31]
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261–5267.
[32]
Kuczynski J, Liu Z, Lozupone C, McDonald D (2010) Microbial community resemblance methods differ in their ability to detect biologically relevant patterns. Nat Methods 7: 813–819.
[33]
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228–8235.
[34]
Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5: 169–172.
[35]
Clarke K, Gorley R (2006) PRIMER v6: User Manual/Tutorial.
[36]
R Development Core Team (2012) R: A Language and Environment for Statistical Computing.
[37]
Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca Species) phyllosphere. Appl Environ Microbiol 76: 8117–8125.
[38]
Telias A, White JR, Pahl DM, Ottesen AR, Walsh CS (2011) Bacterial community diversity and variation in spray water sources and the tomato fruit surface. BMC Microbiol 11: 81.
[39]
Gitaitis RD, Gay JD (1997) First report of a leaf blight, seed stalk rot, and bulb decay of onion by Pantoea ananas in georgia. Plant disease 81: 1096.
[40]
Coutinho TA, Venter SN (2009) Pantoea ananatis: an unconventional plant pathogen. Mol Plant Pathol 10: 325–335.
[41]
Dastager SG, Deepa CK, Puneet SC, Nautiyal CS, Pandey A (2009) Isolation and characterization of plant growth-promoting strain Pantoea NII-186. From Western Ghat Forest soil, India. Lett Appl Microbiol 49: 20–25.
[42]
Wright C, Kominos SD, Yee RB (1976) Enterobacteriaceae and Pseudomonas aeruginosa recovered from vegetable salads. Appl Environ Microbiol 31: 453.
[43]
Abadias M, Usall J, Anguera M, Solsona C, Vi？as I (2008) Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. Int J Food Microbiol 123: 121–129.
[44]
Lindow SE, Brandl MT (2003) Microbiology of the Phyllosphere. Appl Environ Microbiol 69: 1875–1883.
[45]
Smith-Spangler C, Brandeau ML, Hunter GE, Bavinger JC, Pearson M, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157: 348–366.
