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. 2017 Mar 29;284(1851):20162233.
doi: 10.1098/rspb.2016.2233.

Exposure to Dairy Manure Leads to Greater Antibiotic Resistance and Increased Mass-Specific Respiration in Soil Microbial Communities

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Free PMC article

Exposure to Dairy Manure Leads to Greater Antibiotic Resistance and Increased Mass-Specific Respiration in Soil Microbial Communities

Carl Wepking et al. Proc Biol Sci. .
Free PMC article

Abstract

Intensifying livestock production to meet the demands of a growing global population coincides with increases in both the administration of veterinary antibiotics and manure inputs to soils. These trends have the potential to increase antibiotic resistance in soil microbial communities. The effect of maintaining increased antibiotic resistance on soil microbial communities and the ecosystem processes they regulate is unknown. We compare soil microbial communities from paired reference and dairy manure-exposed sites across the USA. Given that manure exposure has been shown to elicit increased antibiotic resistance in soil microbial communities, we expect that manure-exposed sites will exhibit (i) compositionally different soil microbial communities, with shifts toward taxa known to exhibit resistance; (ii) greater abundance of antibiotic resistance genes; and (iii) corresponding maintenance of antibiotic resistance would lead to decreased microbial efficiency. We found that bacterial and fungal communities differed between reference and manure-exposed sites. Additionally, the β-lactam resistance gene ampC was 5.2-fold greater under manure exposure, potentially due to the use of cephalosporin antibiotics in dairy herds. Finally, ampC abundance was positively correlated with indicators of microbial stress, and microbial mass-specific respiration, which increased 2.1-fold under manure exposure. These findings demonstrate that the maintenance of antibiotic resistance associated with manure inputs alters soil microbial communities and ecosystem function.

Keywords: agroecology; ecosystem function; soil ecology.

Figures

Figure 1.
Figure 1.
Fungal and bacterial community composition of soils sourced from reference and manure-exposed (+manure) sites. (a) Principal components analysis showing fungal community composition associated with reference and manure-exposure. Labels indicate the geographical location (i.e. site) for each pair of samples. Permutational MANOVA indicated significant differences between reference and manure-exposed soils. (b) Relative abundance of fungal classes at reference and manure-exposed sites. (c) Principal components analysis showing bacterial community composition associated with reference and manure-exposure. Labels indicate the geographical location (i.e. site) for each pair of samples. Permutational MANOVA indicated significant differences between reference and manure-exposed soils. (d) Relative abundance of bacterial phyla and proteobacterial classes at reference and manure-exposed sites. Note that the difference between site types was primarily due to an increase in the relative abundance of Firmicutes and γ-Proteobacteria.
Figure 2.
Figure 2.
Antibiotic resistance gene (ARG) abundance and the respiratory response to antibiotic additions of soils sourced from reference and manure-exposed (+manure) sites. (a) Abundance of ampC, tetO, tetW and ermB ARGs from reference and manure-exposed sites. ARGs were determined via qPCR. Note that abundance is represented as log gene copies. (b) The natural log of the respiratory response ratio of soils, at reference and manure-exposed sites, exposed to cephapirin, tetracycline or erythromycin. Values above zero indicate an increase in respiration versus a control soil (i.e. no antibiotic addition) and values less than zero indicate a decrease.
Figure 3.
Figure 3.
Relationship between ampC abundance and qCO2, an indicator of microbial stress. Grey circles indicate sites exposed to cattle manure (+manure) and open squares indicate reference sites. A significant relationship was observed for manure-exposed sites but not for reference sites. Additionally, multi-model inference indicates that ampC abundance is an independent variable of high importance when considering microbial stress (electronic supplementary material).
Figure 4.
Figure 4.
The effect of manure-exposure on respiration per unit microbial biomass compared to reference sites. (a) Comparison of respiration per unit microbial biomass (i.e. mass-specific respiration) for manure-exposed and reference sites when amended with water or cephapirin benzathine for 60 days. Significant main effects were noted between manure-exposed and reference sites (F1,30 = 29.13; p < 0.001), as well as between water and cephapirin treatments (F1,30 = 15.60; p < 0.001). We also found a significant interaction between manure exposure and antibiotic amendments (F1,30 = 4.17; p < 0.05). This interaction was due to no difference in mass-specific respiration between antibiotic treatments for the manure-exposed soils but an increase in mass-specific respiration for the reference soil when treated with cephapirin. Notably, the increase in mass-specific respiration from the control to cephapirin treatment we observe for the reference soil is equivalent to what we observe between the reference and manure-exposed soils exposed to water. Letters denote significant pair-wise differences between treatments as determined via Tukey's HSD. Shown are means ± 1 s.e. (b) Mass-specific respiration was positively related to ampC abundance under manure-exposed but not for reference sites.

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