Molecular characterization of Klebsiella pneumoniae resistant to extended-spectrum cephalosporins and carbapenems: a One Health interface

O conceito de “Saúde Única” baseia-se na noção de que a saúde humana, animal e ambiental está intimamente conectada e dependente mutuamente. A Klebsiella pneumoniae, além de colonizar humanos, está presente em diversos hospedeiros e nichos ecológicos como água, solo, plantas e animais. É considerada uma fonte e reservatório de genes de resistência, pelo fato de que, vários genes de resistência antimicrobiana de importância clínica foram descritos pela primeira vez nesta espécie. Sua plasticidade genômica e sua ampla gama ecológica permitem à Klebsiella pneumoniae adquirir, acumular e disseminar facilmente genes de resistência. O objetivo principal deste trabalho foi realizar a caracterização fenotípica e molecular de isolados de Klebsiella pneumoniae resistentes às cefalosporinas de espectro estendido e/ou carbapenêmicos obtidas de diferentes regiões, hospedeiros e nichos ecológicos, a fim de auxiliar na compreensão da distribuição destes microrganismos no Brasil sob a perspectiva de Saúde Única (One Health). Foram coletadas amostras de fezes de humanos da população urbana e rural, swab retal ou cloacal de bovinos, frangos de corte, galinhas (aves) e suínos, amostras de água e solo de propriedades rurais e isolados clínicos de Klebsiella pneumoniae em seis estados brasileiros. Para triagem as amostras foram semeadas em caldo TSB com ceftazidima, ceftriaxona, meropenem (2 µg/mL) e vancomicina (4 µg/mL). Após incubação, as amostras foram semeadas em ágar cromogênico e os isolados obtidos foram identificados pela técnica de MALDI-TOF MS. Os isolados tiveram suas concentrações inibitórias mínimas (CIMs) determinadas para cefalosporinas de espectro estendido e carbapenêmicos, seguindo as recomendações do BrCAST/EUCAST. Para os isolados que apresentaram resistência a estes antimicrobianos, foi realizada a pesquisa de genes que codificam β-lactamases (blaSHV-like, blaTEM-like, blaGES-like, blaCTX-M-1/2-like, blaKPC-like, blaNDM-like, blaIMP-like, blaVIM-like, blaGIM-like, blaSIM-like, blaBKC-like, blaOXA-1-like, blaOXA-2-like, blaOXA-5-like, blaOXA-7/10-like, blaOXA-45-like, blaOXA-46-like e blaOXA-48-like) e determinado seu perfil de similaridade genética por PFGE. Foram coletadas um total de 958 amostras, que após processamento originou 4.383 isolados bacterianos de diferentes espécies. Destes, 318 foram identificados como Klebsiella pneumoniae, sendo 141 (44,33%) sensíveis, 93 (29,24%) resistentes às β-lactamases de espectro estendido e 84 (26,41%) resistentes aos carbapenêmicos. Dos genes codificadores de β-lactamases identificados nos isolados resistentes (N=177), a maior frequência foi do gene blaCTX-M-1/2-like (N=107; 60,45%), seguido pelos genes blaOXA-1-like (N=103; 58,19%), blaTEM-like (N=95; 53,67%), blaKPC-like (76; 42,93%), blaCTX-M-8-like (8; 4,51%), blaCTX-M-14-like (6; 3,38%), blaNDM-like (6; 3,38%), blaOXA-5-like (2; 1,12%) e blaOXA-2-like (1; 0,56%). Observamos uma alta frequência (38,98%) de isolados carreando o contexto genético blaSHV-like, blaTEM-like, blaCTX-M-1/2-like e blaOXA-1-like. Na análise da similaridade genética por PFGE dos isolados recuperados de todos os centros participantes, observamos dois clusters (OH11 e OH21) que agruparam isolados de diferentes regiões, hospedeiros e/ou nichos ecológicos que apresentaram esse mesmo contexto genético. Um isolado clínico recuperado do serviço de saúde do centro de Dourados (MS) com um isolado recuperado de amostras de solo do centro de Castanhal (PA) e um isolado recuperado de amostras de água do centro de Bragança Paulista (SP) com um isolado recuperado de amostras de solo do centro de Castanhal (PA). As análises genômicas realizadas em isolados escolhidos que carreavam esse contexto, mostraram uma alta similaridade dos contigs carreando o gene blaCTX-M-15 e blaOXA-1, os genes estavam em um plasmídeo IncFIB e os clones pertenciam ao clone emergente ST307. Assim, mostramos que clones de Klebsiella pneumoniae com contextos genéticos semelhantes circulam entre diferentes regiões, hospedeiros e nichos ecológicos. Confirmando o papel do solo, águas superficiais e animais de produção como veículos disseminadores de genes de resistência de importância clínica, por apresentarem clones semelhantes com isolados clínicos recuperados neste projeto. Descrevemos também pela primeira vez o gene blaKPC-like e blaOXA-2-like em um suíno. Por fim, destacamos o clone emergente ST307, carreando o contexto blaTEM-like, blaCTX-M-15 e blaOXA-1, como uma nova ameaça à saúde pública no Brasil, tornando a Klebsiella pneumoniae um importante patógeno a ser monitorado pelos programas de vigilância no Brasil sob uma perspectiva de Saúde Única.The concept of "One Health" is based on the notion that human, animal and environmental health are closely connected and mutually dependent. Klebsiella pneumoniae, in addition to colonizing humans, is present in diverse hosts and ecological niches such as water, soil, plants, and animals. It is considered a source and reservoir of resistance genes because several antimicrobial resistance genes of clinical importance have been described for the first time in this species. Its genomic plasticity and wide ecological range allow Klebsiella pneumoniae to easily acquire, accumulate and disseminate resistance genes. The main objective of this work was to perform the phenotypic and molecular characterization of Klebsiella pneumoniae isolates resistant to extendedspectrum cephalosporins and/or carbapenems obtained from different regions, hosts, and ecological niches in order to aid in the understanding of the distribution of these microorganisms in Brazil from a One Health perspective. Stool samples were collected from urban and rural population, rectal or cloacal swab from cattle, broilers, chickens (poultry) and pigs, water and soil samples from rural properties, and clinical isolates of Klebsiella pneumoniae in six Brazilian states. Samples were seeded in TSB broth with ceftazidime, ceftriaxone, meropenem (2 μg/mL) and vancomycin (4 μg/mL) for screening. After incubation, the samples were seeded on chromogenic agar and the isolates obtained were identified by MALDITOF MS technique. The isolates had their minimum inhibitory concentrations (MICs) determined for extended spectrum cephalosporins and carbapenems, following the BrCAST/EUCAST recommendations. For isolates that showed resistance to these antimicrobials, a search for genes encoding βlactamases (blaSHVlike, blaTEMlike, blaGESlike, blaCTXM1/ 2like, blaKPClike, blaNDMlike, blaIMPlike, blaVIMlike, blaGIMlike, blaSIMlike, blaBKClike, blaOXA1like, blaOXA2like, blaOXA5like, blaOXA7/ 10like, blaOXA45like, blaOXA46like, and blaOXA48like) and determined their genetic similarity profile by PFGE. A total of 958 samples were collected, which after processing yielded 4,383 bacterial isolates from different species. Of these, 318 were identified as Klebsiella pneumoniae, of which 141 (44.33%) were susceptible, 93 (29.24%) were resistant to extendedspectrum βlactamases, and 84 (26.41%) were resistant to carbapenems. Of the genes encoding βlactamases identified in the resistant isolates (N=177), the highest frequency was of the blaCTXM1/ 2like gene (N=107; 60.45%), followed by the blaOXA1like genes (N=103; 58.19%), blaTEMlike (N=95; 53.67%), blaKPClike (76; 42.93%), blaCTXM8like (8; 4.51%), blaCTXM14like (6; 3.38%), blaNDMlike (6; 3.38%), blaOXA5like (2; 1.12%), and blaOXA2like (1; 0.56%). We observed a high frequency (38.98%) of isolates carrying the blaSHVlike, blaTEMlike, blaCTXM1/ 2like, and blaOXA1like genetic background. In the PFGE genetic similarity analysis of isolates recovered from all participating centers, we observed two clusters (OH11 and OH21) that grouped isolates from different regions, hosts, and/or ecological niches that showed this same genetic context. A clinical isolate recovered from the health service of the center of Dourados (MS) with an isolate recovered from soil samples from the center of Castanhal (PA) and an isolate recovered from water samples from the center of Bragança Paulista (SP) with an isolate recovered from soil samples from the center of Castanhal (PA). Genomic analyses performed on selected isolates carrying this context showed a high similarity of the contigs carrying the blaCTXM15 and blaOXA1 gene, the genes were on an IncFIB plasmid and the clones belonged to the emerging clone ST307. Thus, we show that Klebsiella pneumoniae clones with similar genetic backgrounds circulate among different regions, hosts and ecological niches. Confirming the role of soil, surface water and farm animals as disseminating vehicles for resistance genes of clinical importance, by presenting similar clones with clinical isolates recovered in this project. We also described for the first time the blaKPClike and blaOXA2like gene in a pig. Finally, we highlight the emerging clone ST307, carrying the blaTEMlike, blaCTXM15 and blaOXA1 context, as a new public health threat in Brazil, making Klebsiella pneumoniae an important pathogen to be monitored by surveillance programs in Brazil under a One Health perspective.Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq

Clonal dissemination of highly virulent Serratia marcescens strains producing KPC-2 in food-producing animals

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) (Process number: 312066/2019-8).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 / Universidade Federal de São Paulo (UNIFESP), 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 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 e Ambiente. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. 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 / 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.Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. Instituto Evandro Chagas. Ananindeua, PA, Brasil.Ministério da Saúde. Secretaria de Vigilância em Saúde e Ambiente. 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 / Universidade Federal de São Paulo (UNIFESP), 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 de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, Brazil.Serratia marcescens is a Gram-negative bacterium presenting intrinsic resistance to polymyxins that has emerged as an important human pathogen. Although previous studies reported the occurrence of multidrug-resistance (MDR) S. marcescens isolates in the nosocomial settings, herein, we described isolates of this extensively drug-resistant (XDR) species recovered from stool samples of food-producing animals in the Brazilian Amazon region. Three carbapenem-resistant S. marcescens strains were recovered from stool samples of poultry and cattle. Genetic similarity analysis showed that these strains belonged to the same clone. Whole-genome sequencing of a representative strain (SMA412) revealed a resistome composed of genes encoding resistance to β-lactams [blaKPC-2, blaSRT-2], aminoglycosides [aac(6′)-Ib3, aac(6′)-Ic, aph(3′)-VIa], quinolones [aac(6′)-Ib-cr], sulfonamides [sul2], and tetracyclines [tet(41)]. In addition, the analysis of the virulome demonstrated the presence of important genes involved in the pathogenicity of this species (lipBCD, pigP, flhC, flhD, phlA, shlA, and shlB). Our data demonstrate that food-animal production can act as reservoirs for MDR and virulent strains of S. marcescens

Clonal dissemination of highly virulent Serratia marcescens strains producing KPC-2 in food-producing animals

Serratia marcescens is a Gram-negative bacterium presenting intrinsic resistance to polymyxins that has emerged as an important human pathogen. Although previous studies reported the occurrence of multidrug-resistance (MDR) S. marcescens isolates in the nosocomial settings, herein, we described isolates of this extensively drug-resistant (XDR) species recovered from stool samples of food-producing animals in the Brazilian Amazon region. Three carbapenem-resistant S. marcescens strains were recovered from stool samples of poultry and cattle. Genetic similarity analysis showed that these strains belonged to the same clone. Whole-genome sequencing of a representative strain (SMA412) revealed a resistome composed of genes encoding resistance to β-lactams [blaKPC-2, blaSRT-2], aminoglycosides [aac(6′)-Ib3, aac(6′)-Ic, aph(3′)-VIa], quinolones [aac(6′)-Ib-cr], sulfonamides [sul2], and tetracyclines [tet(41)]. In addition, the analysis of the virulome demonstrated the presence of important genes involved in the pathogenicity of this species (lipBCD, pigP, flhC, flhD, phlA, shlA, and shlB). Our data demonstrate that food-animal production can act as reservoirs for MDR and virulent strains of S. marcescens

Genomic Analysis of <i>Klebsiella pneumoniae</i> ST258 Strain Coproducing KPC-2 and CTX-M-14 Isolated from Poultry in the Brazilian Amazon Region

This study aimed to characterize a Klebsiella pneumoniae strain (KP411) recovered from the stool samples of poultry (Gallus gallus) in the Brazilian Amazon Region. The whole-genome sequencing of KP411 revealed the presence of an important arsenal of antimicrobial resistance genes to β-lactams (blaCTX-M-14, blaTEM-1B, blaKPC-2, blaSVH-11), aminoglycosides [aph(3″)- Ib, aph(6)-Id, aph(3′)-Ia], sulfonamides (sul1, sul2), quinolones (oqxAB), fosfomycin (fosAKP), and macrolides [mph(A)]. Furthermore, our analyses revealed that the KP411 strain belongs to the ST258 clonal lineage, which is one of the main epidemic clones responsible for the dissemination of KPC-2 worldwide. Our data suggest that food-producing animals may act as reservoirs of multidrug-resistant K. pneumoniae belonging to the ST258 clone, and, consequently, contribute to their dissemination to humans and the environment

Large scale genome-centric metagenomic data from the gut microbiome of food-producing animals and humans

Bill & Melinda Gates Foundation [INV-00764] and CNPq/DECIT [443805/2018-0]; Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio De Janeiro (FAPERJ) E-26/201.046/2022; Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPQ) 307145/2021-2; 312066/2019-8 Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES)National Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, BrazilNational Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, BrazilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, BrazilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, BrazilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, BrazilRegional University of Blumenau. Blumenau, SC, BrazilNational Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, BrazilNational Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, BrazilMinistério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, BrasilMinistério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, BrasilFederal 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. Laboratório de Imunologia e Bacteriologia. Setor de Biologia Molecular, Microbiologia e Imunologia. Diadema, SP, BrazilFederal 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, BrazilUniversity São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, BrazilMinistério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, BrasilUniversidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, BrazilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, BrazilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Alerta. São Paulo, SP, BrazilUniversidade Federal da Grande Dourados. Laboratório de Pesquisa em Ciências da Saúde. Dourados, MS, BrazilUniversity São Francisco. Laboratory of Molecular Biology of Microorganisms. Bragança Paulista, SP, BrazilMinistério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, BrasilUniversidade Federal de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, BrazilUniversidade 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. Laboratório de Imunologia e Bacteriologia. Setor de Biologia Molecular, Microbiologia e Imunologia. 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 de São Paulo. Escola Paulista de Medicina. Department of Internal Medicine. Division of Infectious Diseases. Laboratório Especial de Microbiologia Clínica. São Paulo, SP, BrazilNational Laboratory of Scientific Computing. Bioinformatics Laboratory. Rio de Janeiro, RJ, BrazilThe One Health concept is a global strategy to study the relationship between human and animal health and the transfer of pathogenic and non-pathogenic species between these systems. However, to the best of our knowledge, no data based on One Health genome-centric metagenomics are available in public repositories. Here, we present a dataset based on a pilot-study of 2,915 metagenome-assembled genomes (MAGs) of 107 samples from the human (N = 34), cattle (N = 28), swine (N = 15) and poultry (N = 30) gut microbiomes. Samples were collected from the five Brazilian geographical regions. Of the draft genomes, 1,273 were high-quality drafts (>= 90% of completeness and = 50% of completeness and <= 10% of contamination). Taxonomic predictions were based on the alignment and concatenation of single-marker genes, and the most representative phyla were Bacteroidota, Firmicutes, and Proteobacteria. Many of these species represent potential pathogens that have already been described or potential new families, genera, and species with potential biotechnological applications. Analyses of this dataset will highlight discoveries about the ecology and functional role of pathogens and uncultivated Archaea and Bacteria from food-producing animals and humans. Furthermore, it also represents an opportunity to describe new species from underrepresented taxonomic groups

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