Exploring the bacteriome and resistome of humans and food-producing animals in Brazil

National Council for Science and Technological Development (CNPq) and the Bill & Melinda Gates Foundation (process numbers 402659/2018-0, 443805/2018-0, and OPP1193112); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES); CNPq (process number 312066/2019-8), CNPq (307145/2021-2); FAPERJ (E-26/201.046/2022)National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Regional University of Blumenau. Blumenau, SC, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Federal University of Ceará. Postgraduate Program in Medical Microbiology. Group of Applied Medical Microbiology. Fortaleza, CE, Brazil.Regional University of Blumenau. Blumenau, SC, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.Federal University of Ceará. Postgraduate Program in Medical Microbiology. Group of Applied Medical Microbiology. Fortaleza, CE, Brazil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.University São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil.Universidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, Brazil.University São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Instituto de Ciências Ambientais, Químicas e Farmacêuticas. Departamento de Ciências Biológicas. Setor de Biologia Molecular, Microbiologia e Imunologia. Laboratório de Imunologia e Bacteriologia. Diadema, SP, Brazil.National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, Brazil.Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, Brazil / Universidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.The epidemiology of antimicrobial resistance (AMR) is complex, with multiple interfaces (human-animal-environment). In this context, One Health surveillance is essential for understanding the distribution of microorganisms and antimicrobial resistance genes (ARGs). This report describes a multicentric study undertaken to evaluate the bacterial communities and resistomes of food-producing animals (cattle, poultry, and swine) and healthy humans sampled simultaneously from five Brazilian regions. Metagenomic analysis showed that a total of 21,029 unique species were identified in 107 rectal swabs collected from distinct hosts, the highest numbers of which belonged to the domain Bacteria, mainly Ruminiclostridium spp. and Bacteroides spp., and the order Enterobacterales. We detected 405 ARGs for 12 distinct antimicrobial classes. Genes encoding antibiotic-modifying enzymes were the most frequent, followed by genes related to target alteration and efflux systems. Interestingly, carbapenemase-encoding genes such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1 were identified in distinct hosts. Our results revealed that, in general, the bacterial communities from humans were present in isolated clusters, except for the Northeastern region, where an overlap of the bacterial species from humans and food-producing animals was observed. Additionally, a large resistome was observed among all analyzed hosts, with emphasis on the presence of carbapenemase-encoding genes not previously reported in Latin America. IMPORTANCE Humans and food production animals have been reported to be important reservoirs of antimicrobial resistance (AMR) genes (ARGs). The frequency of these multidrug-resistant (MDR) bacteria tends to be higher in low- and middle-income countries (LMICs), due mainly to a lack of public health policies. Although studies on AMR in humans or animals have been carried out in Brazil, this is the first multicenter study that simultaneously collected rectal swabs from humans and food-producing animals for metagenomics. Our results indicate high microbial diversity among all analyzed hosts, and several ARGs for different antimicrobial classes were also found. As far as we know, we have detected for the first time ARGs encoding carbapenemases, such as blaAIM-1, blaCAM-1, blaGIM-2, and blaHMB-1, in Latin America. Thus, our results support the importance of metagenomics as a tool to track the colonization of food-producing animals and humans by antimicrobial-resistant bacteria. In addition, a network surveillance system called GUARANI, created for this study, is ready to be expanded and to collect additional data