Characterizing the soil microbiome and quantifying antibiotic resistance gene dynamics in agricultural soil following swine CAFO manure application

Lopatto, Edward; Choi, Jinlyung; Colina, Alfredo; Ma, Lanying; Howe, Adina; Hinsa-Leasure, Shannon M.

doi:10.1371/journal.pone.0220770

Cited by 52 publications

(35 citation statements)

References 94 publications

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“…We compared the abundance of intI1, sul1 and tetG in the goat bedding and goat pellet samples with the literature, expecting our results would have a lower prevalence of ARGs compared to reported quantities of ARGs in conventional farms, also known as concentrated animal feeding operations (CAFOs). Instead, we found that our results were on the same order of magnitude of 10 -3 gene copies per 16S rRNA gene for intI1 and tetG in pellets, and a greater order of magnitude for sul1 (Lopatto et al, 2019;Cheng et al, 2013). Since our samples were not actively influenced by antibiotics, but have comparable values to many studies that did use soil influenced by antibiotics, this raises the question of whether antibiotic usage promotes ARGs in microbial populations.…”

Section: Discussioncontrasting

confidence: 47%

Presence and abundance of antibiotic resistance genes at an organic goat dairy farm

Parks

Askew

Creagh-Grave

et al. 2020

IJURCA

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How does the use of antibiotics in animal husbandry impact antibiotic resistance genes (ARGs) and integron prevalence? This article examines the prevalence of nine ARGs (OXA-2, tetB, tetG, blaCMY-2, ereB, NDM, ermB, sul1, and sul2) and two class one integron sequences (intI1 and CS) at an organic goat dairy farm. To provide insight on how antibiotic use is contributing to the abundance of ARGs and integrons outside of where they are used, we made a comparison between our findings and the prevalence of ARGs and integrons at conventional farms from previously published studies. Samples were collected from an organic goat dairy farm in the Willamette Valley from the goat bedding and goat pellets, as well as non-agriculture soil from the Pacific University campus. DNA extraction, followed by PCR and agarose gel electrophoresis, was used to determine the ARG and integron presence in samples. Quantitative PCR was used to determine the ARG and integron abundance in the samples. Out of nine ARGs and two class 1 integron sequences, we found that four ARGs (tetG, ermB, sul1, and sul2) and both class 1 integron sequences (intI1 and CS) were present in the bacterial populations in our samples. tetG, intI1, and sul1 were chosen for qPCR analysis, and revealed equal or higher concentrations when compared to conventional farms. This study highlights the need to compare various practices to determine their impact on ARG prevalence.

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Section: Discussioncontrasting

confidence: 47%

Presence and abundance of antibiotic resistance genes at an organic goat dairy farm

Parks

Askew

Creagh-Grave

et al. 2020

IJURCA

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“…Further microbial community analyses are needed to connect microbial community diversity and ARG attenuation or proliferation, and deeper taxonomic analysis than the genera level may provide insight to potential pathogenicity which will allow for bacterial host identification across the preharvest vegetable production chain. Other studies have indicated need to examine this more closely specifically in agricultural soils (Cycoń et al, 2019;Lopatto et al, 2019) and on vegetable surfaces Shen et al, 2021).…”

Section: Pre-harvest Conditions On Taxonomic Compositionmentioning

confidence: 99%

Integrated Metagenomic Assessment of Multiple Pre-harvest Control Points on Lettuce Resistomes at Field-Scale

et al. 2021

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An integrated understanding of factors influencing the occurrence, distribution, and fate of antibiotic resistance genes (ARGs) in vegetable production systems is needed to inform the design and development of strategies for mitigating the potential for antibiotic resistance propagation in the food chain. The goal of the present study was to holistically track antibiotic resistance and associated microbiomes at three distinct pre-harvest control points in an agroecosystem in order to identify the potential impacts of key agricultural management strategies. Samples were collected over the course of a single growing season (67 days) from field-scale plots amended with various organic and inorganic amendments at agronomic rates. Dairy-derived manure and compost amendment samples (n = 14), soil samples (n = 27), and lettuce samples (n = 12) were analyzed via shotgun metagenomics to assess multiple pre-harvest factors as hypothetical control points that shape lettuce resistomes. Pre-harvest factors of interest included manure collection during/post antibiotic use, manure composting, and soil amended with organic (stockpiled manure/compost) versus chemical fertilizer. Microbial community resistome and taxonomic compositions were unique from amendment to soil to lettuce surface according to dissimilarity analysis. The highest resistome alpha diversity (i.e., unique ARGs, n = 642) was detected in amendment samples prior to soil application, while the composted manure had the lowest total ARG relative abundance (i.e., 16S rRNA gene-normalized). Regardless of amendment type, soils acted as an apparent ecological buffer, i.e., soil resistome and taxonomic profiles returned to background conditions 67 d-post amendment application. Effects of amendment conditions surprisingly re-emerged in lettuce phyllosphere resistomes, with the highest total ARG relative abundances recovered on the surface of lettuce plants grown in organically-fertilized soils (i.e., compost- and manure-amended soils). Co-occurrence analysis identified 55 unique ARGs found both in the soil amendments and on lettuce surfaces. Among these, arnA and pmrF were the most abundant ARGs co-occurring with mobile genetic elements (MGE). Other prominent ARG-MGE co-occurrences throughout this pre-harvest lettuce production chain included: TetM to transposon (Clostridiodies difficile) in the manure amendment and TriC to plasmid (Ralstonia solanacearum) on the lettuce surfaces. This suggests that, even with imposing manure management and post-amendment wait periods in agricultural systems, ARGs originating from manure can still be found on crop surfaces. This study demonstrates a comprehensive approach to identifying key control points for the propagation of ARGs in vegetable production systems, identifying potential ARG-MGE combinations that could inform future surveillance. The findings suggest that additional pre-harvest and potentially post-harvest interventions may be warranted to minimize risk of propagating antibiotic resistance in the food chain.

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“…The microbial populations associated with manure varies due to numerous influential factors, including the producing animal, its feeding regime and the waste management practices (Albihn and Vinnerås, 2007;van Vliet et al, 2007;Jokinen et al, 2012;Lopatto et al, 2019). Manure application can inadvertently spread zoonotic diseases to humans while both animal and plant populations can also be vulnerable to disease (Albihn and Vinnerås, 2007;Spiehs and Goyal, 2007;Longhurst et al, 2019;Tran et al, 2020).…”

Section: Bacteria Manure and Soilmentioning

confidence: 99%

The Fate of Foodborne Pathogens in Manure Treated Soil

et al. 2021

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The aim of this review was to provide an update on the complex relationship between manure application, altered pathogen levels and antibiotic resistance. This is necessary to protect health and improve the sustainability of this major farming practice in agricultural systems based on high levels of manure production. It is important to consider soil health in relation to environment and land management practices in the context of the soil microflora and the introduction of pathogens on the health of the soil microbiome. Viable pathogens in manure spread on agricultural land may be distributed by leaching, surface run-off, water source contamination and contaminated crop removal. Thus it is important to understand how multiple pathogens can persist in manures and on soil at farm-scale and how crops produced under these conditions could be a potential transfer route for zoonotic pathogens. The management of pathogen load within livestock manure is a potential mechanism for the reduction and prevention of outbreaks infection with Escherichia coli, Listeria Salmonella, and Campylobacter. The ability of Campylobacter, E. coli, Listeria and Salmonella to combat environmental stress coupled with their survival on food crops and vegetables post-harvest emphasizes the need for further study of these pathogens along with the emerging pathogen Providencia given its link to disease in the immunocompromised and its’ high levels of antibiotic resistance. The management of pathogen load within livestock manure has been widely recognized as a potential mechanism for the reduction and prevention of outbreaks infection but any studies undertaken should be considered as region specific due to the variable nature of the factors influencing pathogen content and survival in manures and soil. Mediocre soils that require nutrients could be one template for research on manure inputs and their influence on soil health and on pathogen survival on grassland and in food crops.

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Characterizing the soil microbiome and quantifying antibiotic resistance gene dynamics in agricultural soil following swine CAFO manure application

Cited by 52 publications

References 94 publications

Presence and abundance of antibiotic resistance genes at an organic goat dairy farm

Presence and abundance of antibiotic resistance genes at an organic goat dairy farm

Integrated Metagenomic Assessment of Multiple Pre-harvest Control Points on Lettuce Resistomes at Field-Scale

The Fate of Foodborne Pathogens in Manure Treated Soil

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