Long-term impacts of conservation pasture management in manuresheds on system-level microbiome and antibiotic resistance genes

Mitiku Mihiret Seyoum; Amanda J Ashworth; Kristina M Feye; Steven C Ricke; Phillip R Owens; Philip A Moore Jr; Mary Savin

doi:10.3389/fmicb.2023.1227006

Long-term impacts of conservation pasture management in manuresheds on system-level microbiome and antibiotic resistance genes

Front Microbiol. 2023 Sep 29:14:1227006. doi: 10.3389/fmicb.2023.1227006. eCollection 2023.

Authors

Mitiku Mihiret Seyoum¹, Amanda J Ashworth², Kristina M Feye³, Steven C Ricke⁴, Phillip R Owens⁵, Philip A Moore Jr², Mary Savin¹

Affiliations

¹ Department of Crop, Soil, and Environmental Sciences, University of Arkansas, Fayetteville, AR, United States.
² USDA-ARS, Poultry Production and Product Safety Research Unit, Fayetteville, AR, United States.
³ Cellular and Molecular Biology, University of Arkansas, Fayetteville, AR, United States.
⁴ Meat Science & Animal Biologics Discovery Program, Department of Animal and Dairy Sciences, University of Wisconsin-Madison, Madison, WI, United States.
⁵ USDA-ARS, Dale Bumpers Small Farms Research Center, Booneville, AR, United States.

Abstract

Animal manure improves soil fertility and organic carbon, but long-term deposition may contribute to antibiotic resistance genes (ARGs) entering the soil-water environment. Additionally, long-term impacts of applying animal manure to soil on the soil-water microbiome, a crucial factor in soil health and fertility, are not well understood. The aim of this study is to assess: (1) impacts of long-term conservation practices on the distribution of ARGs and microbial dynamics in soil, and runoff; and (2) associations between bacterial taxa, heavy metals, soil health indicators, and ARGs in manures, soils, and surface runoff in a study following 15 years of continuous management. This management strategy consists of two conventional and three conservation systems, all receiving annual poultry litter. High throughput sequencing of the 16S ribosomal RNA was carried out on samples of cattle manure, poultry litter, soil, and runoff collected from each manureshed. In addition, four representative ARGs (intl1, sul1, ermB, and bla_ctx-m-32) were quantified from manures, soil, and runoff using quantitative PCR. Results revealed that conventional practice increased soil ARGs, and microbial diversity compared to conservation systems. Further, ARGs were strongly correlated with each other in cattle manure and soil, but not in runoff. After 15-years of conservation practices, relationships existed between heavy metals and ARGs. In the soil, Cu, Fe and Mn were positively linked to intl1, sul1, and ermB, but trends varied in runoff. These findings were further supported by network analyses that indicated complex co-occurrence patterns between bacteria taxa, ARGs, and physicochemical parameters. Overall, this study provides system-level linkages of microbial communities, ARGs, and physicochemical conditions based on long-term conservation practices at the soil-water-animal nexus.

Keywords: antibiotic resistance genes; cattle manure; heavy metals; microbial communities; poultry litter; runoff.