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.
Highlights
ONE HEALTH AS A COMMUNICATION SPACEA recent reformulation of the classic One Health approach emphasize the role of interconnected ecosystems in the emergence and dissemination of traits that influence local human, animal, plant, and integrated environmental health, such as antibiotic resistance (Knapp et al, 2009; Dandachi et al, 2019; HernandoAmado et al, 2019; Scott et al, 2019; van Bruggen et al, 2019)
One Health is an ecological concept, and antibiotic resistance is a trait linked to microbiotas, microbial assemblages that are organized and evolve by fundamental processes of community ecology (Costello et al, 2012)
Antibiotic-resistant mutants are present in all bacterial populations, and, antibiotic resistance is very ancient in biological times (D’Costa et al, 2011)
Summary
A recent reformulation of the classic One Health approach emphasize the role of interconnected (and geographically close) ecosystems in the emergence and dissemination of traits that influence local human, animal, plant, and integrated environmental health (ecosystem health), such as antibiotic resistance (Knapp et al, 2009; Dandachi et al, 2019; HernandoAmado et al, 2019; Scott et al, 2019; van Bruggen et al, 2019). The current mobile genetic elements (MGEs) carrying antibiotic-resistance genes (as plasmids, transposons, or integrons) were already circulating in Enterobacteriaceae long before the use of antibiotics (Datta and Hughes, 1983; Rowe-Magnus et al, 2001); these elements were rapidly colonized with antibiotic resistance genes, in part evolving from pre-resistance genes, at the time of anthropogenic antibiotic use and selection. It is this utilization that provides a meaning to antibiotic resistance, which allows for communication and the spread of the message, in this case antibiotic resistance. This interaction has greatly increased in the last century, with sociodemographic changes in population, dietary habits, the increase in animal production and meat consumption in low and middle income countries, and the green revolution in agriculture (Tilman, 1998; Tilman et al, 2011; Van Boeckel et al, 2019)
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