Microbiota and Antibiotic Resistome of Lettuce Leaves and Radishes Grown in Soils Receiving Manure-Based Amendments Derived From Antibiotic-Treated Cows

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dc.contributor.authorFogler, Kendallen
dc.contributor.authorGuron, Giselle K.P.en
dc.contributor.authorWind, Lauren L.en
dc.contributor.authorKeenum, Ishi M.en
dc.contributor.authorHession, W. Cullyen
dc.contributor.authorKrometis, Leigh-Anne H.en
dc.contributor.authorStrawn, Laura K.en
dc.contributor.authorPruden, Amyen
dc.contributor.authorPonder, Monica A.en
dc.contributor.departmentCivil and Environmental Engineeringen
dc.contributor.departmentBiological Systems Engineeringen
dc.contributor.departmentFood Science and Technologyen
dc.date.accessioned2019-11-13T13:49:24Zen
dc.date.available2019-11-13T13:49:24Zen
dc.date.issued2019-04-10en
dc.description.abstractCattle are commonly administered antibiotics, resulting in excretion of antibiotics, antibiotic-resistant bacteria (ARB), and antibiotic resistance genes (ARGs). The aim of this study was to determine if the use of dairy manure collected during antibiotic administration influences the bacterial microbiota of lettuce and radishes, including carriage of ARB and ARGs, when applied as a soil amendment and if composting mitigates the effects. Lettuce and radishes were grown in field-plots amended with raw manure from antibiotic-treated (cephapirin, pirlimycin) cows, composted manure from antibiotic-treated cows, composted manure from antibiotic-free cows, or an inorganic chemical fertilizer (control; 12 plots, n = 3). Surficial vegetable bacteria and antibiotic resistomes (i.e., total ARGs) were characterized using heterotrophic plate counts (HPCs) on antibiotic-containing media, 16S rRNA gene amplicon sequencing, quantitative polymerase chain reaction (qPCR), and shot-gun metagenomics. The different manure and compost amendments did not result in significant changes to the surficial vegetable bacteria at the phylum level; however, some minor changes at the class and family level were observed. Beta-diversities of the ARGs detected by shotgun metagenomic sequencing were distinctly different between vegetable type (R = 0.30, p = 0.04), with small separations between the resistomes associated with amendment type in unrarefied analysis (R = 0.27, p = 0.02), but not rarefied analysis, of the data. Network analysis highlighted that multi-drug ARG classes commonly co-occurred with plasmid-associated genes and could be a driver of co-and cross-selection of ARGs in the different conditions. Carriage of sul1 and tet(W) ARGs on vegetables quantified by qPCR were strong indicators of manure-based amendment relative to chemical fertilizer, with some reduction incurred via composting (p < 0.05). Also, increased HPCs resistant/tolerant to clindamycin, a class of antibiotics administered to cattle, were on lettuce grown in biological soil amendments relative to chemical fertilizer (p < 0.05). This study demonstrates that amending soil with rawmanure collected fromdairy cows during antibiotic administration may affect the composition of microbiota and resistomes associated with vegetable surfaces. Composting may be an important strategy to reduce some ARGs on fresh produce, but differences in the resistomes of lettuce and radishes suggest the extent of soil contact should be considered.en
dc.description.sponsorshipThis work was supported by the USDA NIFA-AFRI 2014-05280/2015-68003-23050 awards and the Virginia Agricultural Experiment Station and the Hatch Program of the National Institute of Food and Agriculture, U.S. Department of Agriculture.en
dc.format.extent17 pagesen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationFogler K, Guron GKP, Wind LL, Keenum IM, Hession WC, Krometis L-A, Strawn LK, Pruden A and Ponder MA (2019) Microbiota and Antibiotic Resistome of Lettuce Leaves and Radishes Grown in Soils Receiving Manure-Based Amendments Derived From Antibiotic-Treated Cows. Front. Sustain. Food Syst. 3:22. doi: 10.3389/fsufs.2019.00022en
dc.identifier.doihttps://doi.org/10.3389/fsufs.2019.00022en
dc.identifier.urihttp://hdl.handle.net/10919/95521en
dc.identifier.volume3en
dc.language.isoenen
dc.publisherFrontiersen
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjectantibiotic resistance genesen
dc.subjectphyllosphere bacteriaen
dc.subjectmetagenomicsen
dc.subjectvegetable productionen
dc.subjectnetwork analysisen
dc.titleMicrobiota and Antibiotic Resistome of Lettuce Leaves and Radishes Grown in Soils Receiving Manure-Based Amendments Derived From Antibiotic-Treated Cowsen
dc.title.serialFrontiers in Sustainable Food Systemsen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
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Destination Area: Global Systems Science (GSS)
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