Antibiotic Resistance Gene Diversity and Virulence Gene Diversity Are Correlated in Human Gut and Environmental Microbiomes.

Pedro Escudeiro,Teresa Nogueira,Francisco Dionisio,Joël Pothier,Paul D Fey

doi:10.1128/msphere.00135-19

Abstract

Human beings have used large amounts of antibiotics, not only in medical contexts but also, for example, as growth factors in agriculture and livestock, resulting in the contamination of the environment. Even when pathogenic bacteria are the targets of antibiotics, hundreds of nonpathogenic bacterial species are affected as well. Therefore, both pathogenic and nonpathogenic bacteria have gradually become resistant to antibiotics. We tested whether there is still cooccurrence of resistance and virulence determinants. We performed a comparative study of environmental and human gut metagenomes from different individuals and from distinct human populations across the world. We found a great diversity of antibiotic resistance determinants (AR diversity [ARd]) and virulence factors (VF diversity [VFd]) in metagenomes. Importantly there is a correlation between ARd and VFd, even after correcting for protein family richness. In the human gut, there are less ARd and VFd than in more diversified environments, and yet correlations between the ARd and VFd are stronger. They can vary from very high in Malawi, where antibiotic consumption is unattended, to nonexistent in the uncontacted Amerindian population. We conclude that there is cooccurrence of resistance and virulence determinants in human gut microbiomes, suggesting a possible coselective mechanism.IMPORTANCE Every year, thousands of tons of antibiotics are used, not only in human and animal health but also as growth promoters in livestock. Consequently, during the last 75 years, antibiotic-resistant bacterial strains have been selected in human and environmental microbial communities. This implies that, even when pathogenic bacteria are the targets of antibiotics, hundreds of nonpathogenic bacterial species are also affected. Here, we performed a comparative study of environmental and human gut microbial communities issuing from different individuals and from distinct human populations across the world. We found that antibiotic resistance and pathogenicity are correlated and speculate that, by selecting for resistant bacteria, we may be selecting for more virulent strains as a side effect of antimicrobial therapy.

Highlights

Human beings have used large amounts of antibiotics, in medical contexts and, for example, as growth factors in agriculture and livestock, resulting in the contamination of the environment
We show that there is a linkage between the dissemination of virulence factors and genes coding for antibiotic resistance, within natural microbiomes, and that this relationship could be influenced by the behaviors of human populations spanning very different geographical locations across the world
Antibiotic Resistance and Virulence in Microbiomes the metagenome protein family richness? To answer this question, we used a data set composed of natural metagenomes issuing from diverse ecosystems and biomes, such as oceans, coral atolls, deep oceans, Antarctic aquatic environments and snow, soils, hypersaline sediments, sludges, microbial fuel cell biofilms, and animal microbial populations [25], and which on will be referred to here as environmental metagenomes, in contrast to those composed solely of human gut metagenomes

Summary

Introduction

Human beings have used large amounts of antibiotics, in medical contexts and, for example, as growth factors in agriculture and livestock, resulting in the contamination of the environment. During the last 75 years, antibiotic-resistant bacterial strains have been selected in human and environmental microbial communities. This implies that, even when pathogenic bacteria are the targets of antibiotics, hundreds of nonpathogenic bacterial species are affected. We performed a comparative study of environmental and human gut microbial communities issuing from different individuals and from distinct human populations across the world. If antibiotic resistance genes are carried by plasmids or other mobile genetic elements, they may transfer to pathogenic cells and save them from the negative effects of antibiotics These genetic elements can spread into the bacterial community by horizontal gene transfer, even crossing species [12,13,14]. They are able to amplify the number of plasmids in a bacterial community and spread those plasmids to other bacterial cells [15], a phenomenon probably explained by interactions between different plasmids [16, 17]

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