Comparing gut resistome composition among patients with acute Campylobacter infections and healthy family members

Walid Khalife,Duane W Newton,Brian Nohomovich,Shannon D Manning,Ashley Shade,Paul Lephart,Hossein Salimnia,James T Rudrik,Zoe A Hansen,Wonhee Cha

doi:10.1038/s41598-021-01927-7

Abstract

Campylobacter commonly causes foodborne infections and antibiotic resistance is an imminent concern. It is not clear, however, if the human gut ‘resistome’ is affected by Campylobacter during infection. Application of shotgun metagenomics on stools from 26 cases with Campylobacter infections and 44 healthy family members (controls) identified 406 unique antibiotic resistance genes (ARGs) representing 153 genes/operons, 40 mechanisms, and 18 classes. Cases had greater ARG richness (p < 0.0001) and Shannon diversity (p < 0.0001) than controls with distinct compositions (p = 0.000999; PERMANOVA). Cases were defined by multidrug resistance genes and were dominated by Proteobacteria (40.8%), specifically those representing Escherichia (20.9%). Tetracycline resistance genes were most abundant in controls, which were dominated by Bacteroidetes (45.3%) and Firmicutes (44.4%). Hierarchical clustering of cases identified three clusters with distinct resistomes. Case clusters 1 and 3 differed from controls containing more urban and hospitalized patients. Relative to family members of the same household, ARG composition among matched cases was mostly distinct, though some familial controls had similar profiles that could be explained by a shorter time since exposure to the case. Together, these data indicate that Campylobacter infection is associated with an altered resistome composition and increased ARG diversity, raising concerns about the role of infection in the spread of resistance determinants.

Highlights

Campylobacter commonly causes foodborne infections and antibiotic resistance is an imminent concern
In 2018, the Centers for Disease Control and Prevention (CDC) reported that the incidence of foodborne infection was highest for Campylobacter and Salmonella, with the incidence of both pathogens increasing relative to the frequencies reported in 2015–20172
We found that gut communities characterized from the stools of patients with Campylobacter infections had increased resistome diversity relative to healthy family members

Summary

Introduction

Campylobacter commonly causes foodborne infections and antibiotic resistance is an imminent concern. Relative to family members of the same household, ARG composition among matched cases was mostly distinct, though some familial controls had similar profiles that could be explained by a shorter time since exposure to the case Together, these data indicate that Campylobacter infection is associated with an altered resistome composition and increased ARG diversity, raising concerns about the role of infection in the spread of resistance determinants. Further consideration and characterization of the ecological consequences of enteric infection in the human gut microbiome is needed In addition to their role in causing foodborne illness, Campylobacter spp., are progressively found to be drug-resistant, which has led to their classification as a serious public health threat by the C DC4. Elucidating the impacts of ecological invasion on the composition and mobility of ARGs in the human gut is crucial to advancing our fight against the spread of drug resistance

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