Gene Transmission in the One Health Microbiosphere and the Channels of Antimicrobial Resistance

Abstract

Antibiotic resistance is a field in which the concept of One Health can best be illustrated. One Health is based on the definition of communication spaces among diverse environments. Antibiotic resistance is encoded by genes, however, these genes are propagated in mobile genetic elements (MGEs), circulating among bacterial species and clones that are integrated into the multiple microbiotas of humans, animals, food, sewage, soil, and water environments, the One Health microbiosphere. The dynamics and evolution of antibiotic resistance depend on the communication networks linking all these ecological, biological, and genetic entities. These communications occur by environmental overlapping and merging, a critical issue in countries with poor sanitation, but also favored by the homogenizing power of globalization. The overwhelming increase in the population of highly uniform food animals has contributed to the parallel increase in the absolute size of their microbiotas, consequently enhancing the possibility of microbiome merging between humans and animals. Microbial communities coalescence might lead to shared microbiomes in which the spread of antibiotic resistance (of human, animal, or environmental origin) is facilitated. Intermicrobiome communication is exerted by shuttle bacterial species (or clones within species) belonging to generalist taxa, able to multiply in the microbiomes of various hosts, including humans, animals, and plants. Their integration into local genetic exchange communities fosters antibiotic resistance gene flow, following the channels of accessory genome exchange among bacterial species. These channels delineate a topology of gene circulation, including dense clusters of species with frequent historical and recent exchanges. The ecological compatibility of these species, sharing the same niches and environments, determines the exchange possibilities. In summary, the fertility of the One Health approach to antibiotic resistance depends on the progress of understanding multihierarchical systems, encompassing communications among environments (macro/microaggregates), among microbiotas (communities), among bacterial species (clones), and communications among MGEs.

Keywords: accessory genes; gene flow channels; microbiome merging; one health; resistance genes.

FIGURE 1

Bipartite network illustrating the accessory genes (proteins) gene flow among species of the major taxons of Gamma-Proteobacteria. Connections between bacterial species indicates that the same accessory gene is shared by both. The distance between species (genus, in italics) is proportional to the number of connections. On the right, detail of the “core” of Enterobacteriaceae species sharing accessory genes. Flow of antibiotic resistance genes should correspond to the flow of accessory genes. “Trumpet-like” patterns on the surface of some clusters correspond to accessory genes that are unique for a particular strain (not connected with any other). Reproduced with permission from Lanza et al. (2018).

FIGURE 2

Multilevel communication between environments influencing antibiotic resistance. Communication occurs among environments (red circles and large red “communication” triangle), among the microbiotas contained in these environments (yellow circles y large yellow triangle), and among the species and clones contained in these microbiotas (blue circles and blue triangle). Inside environments there are spatially defined subenvironments or macroaggregates (light blue small circles). They contain microbiotas, bacterial community microaggregates (pink circles), which at their turn contain bacterial species and clones (light gray circles), which contain mobile genetic elements (rings, representing plasmids). At each one of these levels, communications (small triangles) are established. One Health emphasized that merging of environments, microbiotas, and bacterial communities, favors communications and consequently the spread of antibiotic resistance genes.