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ARS Home » Midwest Area » Ames, Iowa » National Animal Disease Center » Food Safety and Enteric Pathogens Research » Research » Publications at this Location » Publication #324680

Title: Clusters of antibiotic resistance genes enriched together stay together in swine agriculture

item JOHNSON, TIMOTHY - Orise Fellow
item STEDTFELD, ROBERT - Michigan State University
item WANG, QIONG - Michigan State University
item COLE, JAMES - Michigan State University
item HASHSHAM, SYED - Michigan State University
item Looft, Torey
item ZHU, YONG-GUAN - Chinese Academy Of Sciences
item TIEDJE, JAMES - Michigan State University

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/8/2016
Publication Date: 4/12/2016
Citation: Johnson, T.A., Stedtfeld, R.D., Wang, Q., Cole, J.R., Hashsham, S.A., Looft, T.P., Zhu, Y., Tiedje, J.M. 2016. Antibiotic resistance genes enriched together stay together: Lessons from swine agriculture. mBio. 7(2):e02214-02215. doi: 10.1128/mBio.02214-02215.

Interpretive Summary: Antibiotic-resistant bacteria are a global health concern that causes an estimated $20 billion in health care costs each year. Tracking the source of antibiotic resistance is a very complicated issue because antibiotic use (which increases the occurrence of resistance) is widespread, and antibiotic resistance can spread between bacteria. Studies have shown that antibiotic resistance genes can be found in different types of bacteria in all environments examined. This widespread distribution is due to their presence on mobile genetic elements, which allow bacteria to share their antibiotic resistance genes with their bacterial neighbors. Agricultural antibiotic use increases the abundance of resistance genes and mobile genetic elements. In this study, we examined both these types of genes in bacterial deoxyribonucleic acid (DNA) from Chinese swine farms and United States laboratory swine to assess the relationship between resistance genes and mobile genetic elements. We found that many resistance genes and mobile genetic elements are found together, meaning when one gene increased or decreased in abundance, partner genes increased or decreased in nearly identical fashion. Our results indicate that on the Chinese farms, the potential for widespread resistance gene transfer among environmental bacteria is high. Taken together, our results show in a clear manner: the diversity of resistance genes on swine farms; that many genes likely originated from the same source (due to identical sequences); and the broad linkage of resistance genes to each other as well as to genes that enable them to be shared among bacteria. These findings will help guide lawmakers in developing policies for prudent agricultural antibiotic use and to prevent antibiotic resistance genes spreading to other bacteria.

Technical Abstract: Antibiotic resistance has developed into a worldwide health risk. The nature and extent of the contribution of animal agriculture to the evolution of antibiotic resistance in bacterial communities remains unclear. Using quantitative polymerase chain reaction (PCR) in tandem with next-generation sequencing, we quantified and sequenced 44 genes related to antibiotic resistance, mobile genetic elements (MGE) and bacterial phylogeny in United States laboratory swine and Chinese swine farms. Resistance clusters were identified, which are groups of the most abundant amplicon sequences of resistance and mobile genetic element genes that statistically co-occur. Identical resistance clusters were identified throughout geographically distant Chinese farms largely independent of phylogenetic composition of the bacterial communities. Resistance genes were enriched and statistically co-occur in the laboratory swine that confer resistance to antibiotics that were and were not feed to the animals and their co-localization in bacterial genomes is a likely mechanism of their co-enrichment. One Chinese resistance cluster contained resistance genes to six classes of antibiotics together with class 1 integrase (intI1), is6100 type transposons, and incW broad host range plasmids. This observation is consistent with enrichment of multi-gene resistance islands or plasmids. Eight of the 15 sequences from this Chinese resistance cluster aligned with 100 percent identity in co-localized clusters in a known bacterial resistance island. Together, our findings suggest animal agriculture as an environment that selects for the co-enrichment and co-occurrence of multiple antibiotic resistance genes and mobile genetic elements, and highlight a critical need to understand the genetic context of both gene types and their dissemination throughout bacterial communities.