Cross-Sectional Analysis of the Microbiota of Human Gut and Its Direct Environment in a Household Cohort with High Background of Antibiotic Use

Comprehensive insight into the microbiota of the gut of humans and animals, as well as their living environment, in communities with a high background of antibiotic use and antibiotic resistance genes is scarce. Here, we used 16S rRNA gene sequencing to describe the (dis)similarities in the microbiota of feces from humans (n = 107), domestic animals (n = 36), water (n = 89), and processed food (n = 74) in a cohort with individual history of antibiotic use in northern Vietnam. A significantly lower microbial diversity was observed among individuals who used antibiotics in the past 4 months (n = 44) compared to those who did not (n = 63). Fecal microbiota of humans was more diverse than nonhuman samples and shared a small part of its amplicon sequence variants (ASVs) with feces from animals (7.4% (3.2–9.9)), water (2.2% (1.2–2.8)), and food (3.1% (1.5–3.1)). Sharing of ASVs between humans and companion animals was not associated with the household. However, we did observe a correlation between an Enterobacteriaceae ASV and the presence of extended-spectrum beta-lactamase CTX-M-group-2 encoding genes in feces from humans and animals (p = 1.6 × 10−3 and p = 2.6 × 10−2, respectively), hinting toward an exchange of antimicrobial-resistant strains between reservoirs.

[1]  G. Kowalchuk,et al.  A global overview of the trophic structure within microbiomes across ecosystems. , 2021, Environment international.

[2]  Suisha Liang,et al.  Impact of outdoor nature-related activities on gut microbiota, fecal serotonin, and perceived stress in preschool children: the Play&Grow randomized controlled trial , 2020, Scientific Reports.

[3]  E. Bezirtzoglou,et al.  Effects of Antibiotics upon the Gut Microbiome: A Review of the Literature , 2020, Biomedicines.

[4]  P. Savelkoul,et al.  How to Count Our Microbes? The Effect of Different Quantitative Microbiome Profiling Approaches , 2020, Frontiers in Cellular and Infection Microbiology.

[5]  Charlene C. Nielsen,et al.  Natural environments in the urban context and gut microbiota in infants. , 2020, Environment international.

[6]  G. Gao,et al.  Metagenomic analysis reveals the microbiome and resistome in migratory birds , 2020, Microbiome.

[7]  J. Carlin,et al.  Gut microbiota composition during infancy and subsequent behavioural outcomes , 2020, EBioMedicine.

[8]  Shenghui Li,et al.  Characterization of the Pig Gut Microbiome and Antibiotic Resistome in Industrialized Feedlots in China , 2019, mSystems.

[9]  Pham Duy Thai,et al.  An exploration of the gut and environmental resistome in a community in northern Vietnam in relation to antibiotic use , 2019, Antimicrobial Resistance & Infection Control.

[10]  N. Neff,et al.  Recovery of the Gut Microbiota after Antibiotics Depends on Host Diet, Community Context, and Environmental Reservoirs. , 2019, Cell host & microbe.

[11]  B. Zhu,et al.  An examination of data from the American Gut Project reveals that the dominance of the genus Bifidobacterium is associated with the diversity and robustness of the gut microbiota , 2019, MicrobiologyOpen.

[12]  Vineet K. Sharma,et al.  Metagenome of a polluted river reveals a reservoir of metabolic and antibiotic resistance genes , 2019, Environmental Microbiome.

[13]  B. Pulendran,et al.  Antibiotics-Driven Gut Microbiome Perturbation Alters Immunity to Vaccines in Humans , 2019, Cell.

[14]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[15]  B. Bohannan,et al.  Population Genetic Divergence and Environment Influence the Gut Microbiome in Oregon Threespine Stickleback , 2019, Genes.

[16]  J. Morris,et al.  One Health - Cycling of diverse microbial communities as a connecting force for soil, plant, animal, human and ecosystem health. , 2019, The Science of the total environment.

[17]  E. Topp,et al.  Environmental risk assessment of antibiotics in agroecosystems: ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum , 2019, Environmental Science and Pollution Research.

[18]  G. Cochrane,et al.  Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage , 2019, Nature Communications.

[19]  M. Yasir,et al.  Association of gut dysbiosis with intestinal metabolites in response to antibiotic treatment , 2019, Human Microbiome Journal.

[20]  Karsten Zengler,et al.  A Novel Sparse Compositional Technique Reveals Microbial Perturbations , 2019, mSystems.

[21]  Xiaosong Hu,et al.  Resveratrol-induced gut microbiota reduces obesity in high-fat diet-fed mice , 2019, International Journal of Obesity.

[22]  A. Gasbarrini,et al.  What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases , 2019, Microorganisms.

[23]  Paul Theodor Pyl,et al.  Recovery of gut microbiota of healthy adults following antibiotic exposure , 2018, Nature Microbiology.

[24]  F. Balloux,et al.  Modelling microbiome recovery after antibiotics using a stability landscape framework , 2018, bioRxiv.

[25]  H. V. van Doorn,et al.  Antibiotic consumption in low-income and middle-income countries. , 2018, Lancet Global Health.

[26]  Eeva Furman,et al.  The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems. , 2018, The Science of the total environment.

[27]  Rob Knight,et al.  Current understanding of the human microbiome , 2018, Nature Medicine.

[28]  Nhung Dang,et al.  Antibiotics in the aquatic environment of Vietnam: Sources, concentrations, risk and control strategy. , 2018, Chemosphere.

[29]  Rob Knight,et al.  Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania , 2017, Science.

[30]  Paul J. McMurdie,et al.  Exact sequence variants should replace operational taxonomic units in marker-gene data analysis , 2017, The ISME Journal.

[31]  F. Raymond,et al.  Partial recovery of microbiomes after antibiotic treatment , 2016, Gut microbes.

[32]  D. van Sinderen,et al.  Bifidobacteria and Their Role as Members of the Human Gut Microbiota , 2016, Front. Microbiol..

[33]  R. Osawa,et al.  Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study , 2016, BMC Microbiology.

[34]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[35]  Molly K. Gibson,et al.  Developmental dynamics of the preterm infant gut microbiota and antibiotic resistome , 2016, Nature Microbiology.

[36]  A. Stallmach,et al.  Effects of Antibiotics on Gut Microbiota , 2016, Digestive Diseases.

[37]  G. Ko,et al.  Sellimonas intestinalis gen. nov., sp. nov., isolated from human faeces. , 2016, International journal of systematic and evolutionary microbiology.

[38]  F. Raymond,et al.  The initial state of the human gut microbiome determines its reshaping by antibiotics , 2015, The ISME Journal.

[39]  Rob Knight,et al.  Analysis of composition of microbiomes: a novel method for studying microbial composition , 2015, Microbial ecology in health and disease.

[40]  Rob Knight,et al.  The microbiome of uncontacted Amerindians , 2015, Science Advances.

[41]  E. De Pauw,et al.  Monitoring Antibiotic Use and Residue in Freshwater Aquaculture for Domestic Use in Vietnam , 2015, EcoHealth.

[42]  J. Escobar,et al.  The gut microbiota of Colombians differs from that of Americans, Europeans and Asians , 2014, BMC Microbiology.

[43]  K. Swanson,et al.  Gut microbiota of humans, dogs and cats: current knowledge and future opportunities and challenges , 2014, British Journal of Nutrition.

[44]  L. Boon,et al.  The combination of Bifidobacterium breve with non-digestible oligosaccharides suppresses airway inflammation in a murine model for chronic asthma. , 2014, Biochimica et biophysica acta.

[45]  P. Horby,et al.  Antibiotic sales in rural and urban pharmacies in northern Vietnam: an observational study , 2014, BMC Pharmacology and Toxicology.

[46]  Se Jin Song,et al.  Cohabiting family members share microbiota with one another and with their dogs , 2013, eLife.

[47]  L. Soleo,et al.  Environmental Contamination by Dog’s Faeces: A Public Health Problem? , 2012, International journal of environmental research and public health.

[48]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[49]  P. Pochart,et al.  Long-Term Changes in Human Colonic Bifidobacterium Populations Induced by a 5-Day Oral Amoxicillin-Clavulanic Acid Treatment , 2012, PloS one.

[50]  R. Knight,et al.  Diversity, stability and resilience of the human gut microbiota , 2012, Nature.

[51]  Tari Haahtela,et al.  Environmental biodiversity, human microbiota, and allergy are interrelated , 2012, Proceedings of the National Academy of Sciences.

[52]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[53]  D. Relman,et al.  Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation , 2010, Proceedings of the National Academy of Sciences.

[54]  S. Massart,et al.  Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa , 2010, Proceedings of the National Academy of Sciences.

[55]  Anders F. Andersson,et al.  Short-Term Antibiotic Treatment Has Differing Long-Term Impacts on the Human Throat and Gut Microbiome , 2010, PloS one.

[56]  Paramvir S. Dehal,et al.  FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments , 2010, PloS one.

[57]  J. Doré,et al.  Differences in Fecal Microbiota in Different European Study Populations in Relation to Age, Gender, and Country: a Cross-Sectional Study , 2006, Applied and Environmental Microbiology.

[58]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[59]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[60]  T. V. Dinh,et al.  First Survey on the Use of Antibiotics in Pig and Poultry Production in the Red River Delta Region of Vietnam , 2013 .

[61]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .

[62]  A. Chao Nonparametric estimation of the number of classes in a population , 1984 .

[63]  J. Atchison,et al.  Logistic-normal distributions:Some properties and uses , 1980 .