Anna T Nguyen, Kalani Ratnasiri, Gabriella Barratt Heitmann, Sumaiya Tazin, Claire Anderson, Suhi Hanif, Afsana Yeamin, Abul Kasham Shoab, Ireen Sultana Shanta, Farjana Jahan, Md Sakib Hossain, Zahid Hayat Mahmud, Mohammad Jubair, Mustafizur Rahman, Mahbubur Rahman, Ayse Ercumen, Jade Benjamin-Chung
{"title":"家庭环境中的潜在病原体和抗微生物药物耐药性基因:对孟加拉国农村土壤地面和牛粪的研究","authors":"Anna T Nguyen, Kalani Ratnasiri, Gabriella Barratt Heitmann, Sumaiya Tazin, Claire Anderson, Suhi Hanif, Afsana Yeamin, Abul Kasham Shoab, Ireen Sultana Shanta, Farjana Jahan, Md Sakib Hossain, Zahid Hayat Mahmud, Mohammad Jubair, Mustafizur Rahman, Mahbubur Rahman, Ayse Ercumen, Jade Benjamin-Chung","doi":"10.1128/aem.00669-25","DOIUrl":null,"url":null,"abstract":"<p><p>In low- and middle-income countries, living in homes with soil floors and animal cohabitation may expose children to fecal organisms, increasing the risk of enteric and antimicrobial-resistant infections. Our objective was to understand whether cow cohabitation in homes with soil floors in rural Bangladesh contributed to the presence and diversity of potential pathogens and antimicrobial resistance genes (ARGs) in the home. In 10 randomly selected households in rural Sirajganj District, we sampled floor soil and cow dung, which is commonly used as sealant in soil floors. We extracted DNA and performed shotgun metagenomic sequencing to explore potential pathogens and ARGs in each sample type. We detected 7 potential pathogens in soil only, 38 pathogens in cow dung only, and 182 pathogens in both soil and cow dung. Cow dung exhibited modestly higher potential pathogen genus richness compared to soil floors (Wilcoxon signed-rank test, <i>P</i> = 0.002). Using Bray-Curtis dissimilarity, potential pathogen species community composition differed between floors and cow dung (permutational multivariate analysis of variance, <i>P</i> < 0.001). All soil floor and cow dung samples contained ARGs; detected ARGs confer resistance to antibiotic classes including sulfonamides, rifamycin, aminoglycosides, lincosamides, and tetracycline. Paired floor and cow dung samples shared ARGs against rifamycin and glycopeptides, but otherwise, there was little overlap in resistomes between sample types. Our findings contribute to the growing literature on household soil and domestic animals as potentially important contributors to disease transmission and as reservoirs of antimicrobial resistance in low-income country settings.IMPORTANCEIn low-income countries, inadequate housing materials and animal cohabitation can lead to fecal contamination of rural homes. Contaminated soil floors are difficult to clean and may harbor organisms causing illness and antibiotic resistance, especially in young children, who frequently ingest soil. We sequenced soil floor and cow dung samples from households in Sirajganj district, Bangladesh, and identified potential pathogens and antibiotic resistance genes. We detected 182 potential pathogens in both soil and cow dung; organisms present in both sample types at the highest relative abundances were <i>Escherichia coli</i>, <i>Klebsiella pneumoniae, Salmonella enterica</i>, and <i>Pseudomonas aeruginosa</i>. Antibiotic resistance genes were found in all samples. In cow dung, the most common genes conferred resistance to the antibiotics lincosamide, rifamycin, cephamycin, tetracycline, and multiple antibiotics. In soil floors, the most common genes conferred resistance to rifamycin, sulfonamides, and multiple antibiotics. Household soil and cow dung may be important reservoirs of pathogens and antimicrobial resistance in low-income country settings with high levels of animal cohabitation compared to settings with finished household floors and minimal animal cohabitation.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0066925"},"PeriodicalIF":3.7000,"publicationDate":"2025-06-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12175521/pdf/","citationCount":"0","resultStr":"{\"title\":\"Potential pathogens and antimicrobial resistance genes in household environments: a study of soil floors and cow dung in rural Bangladesh.\",\"authors\":\"Anna T Nguyen, Kalani Ratnasiri, Gabriella Barratt Heitmann, Sumaiya Tazin, Claire Anderson, Suhi Hanif, Afsana Yeamin, Abul Kasham Shoab, Ireen Sultana Shanta, Farjana Jahan, Md Sakib Hossain, Zahid Hayat Mahmud, Mohammad Jubair, Mustafizur Rahman, Mahbubur Rahman, Ayse Ercumen, Jade Benjamin-Chung\",\"doi\":\"10.1128/aem.00669-25\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>In low- and middle-income countries, living in homes with soil floors and animal cohabitation may expose children to fecal organisms, increasing the risk of enteric and antimicrobial-resistant infections. Our objective was to understand whether cow cohabitation in homes with soil floors in rural Bangladesh contributed to the presence and diversity of potential pathogens and antimicrobial resistance genes (ARGs) in the home. In 10 randomly selected households in rural Sirajganj District, we sampled floor soil and cow dung, which is commonly used as sealant in soil floors. We extracted DNA and performed shotgun metagenomic sequencing to explore potential pathogens and ARGs in each sample type. We detected 7 potential pathogens in soil only, 38 pathogens in cow dung only, and 182 pathogens in both soil and cow dung. Cow dung exhibited modestly higher potential pathogen genus richness compared to soil floors (Wilcoxon signed-rank test, <i>P</i> = 0.002). Using Bray-Curtis dissimilarity, potential pathogen species community composition differed between floors and cow dung (permutational multivariate analysis of variance, <i>P</i> < 0.001). All soil floor and cow dung samples contained ARGs; detected ARGs confer resistance to antibiotic classes including sulfonamides, rifamycin, aminoglycosides, lincosamides, and tetracycline. Paired floor and cow dung samples shared ARGs against rifamycin and glycopeptides, but otherwise, there was little overlap in resistomes between sample types. Our findings contribute to the growing literature on household soil and domestic animals as potentially important contributors to disease transmission and as reservoirs of antimicrobial resistance in low-income country settings.IMPORTANCEIn low-income countries, inadequate housing materials and animal cohabitation can lead to fecal contamination of rural homes. Contaminated soil floors are difficult to clean and may harbor organisms causing illness and antibiotic resistance, especially in young children, who frequently ingest soil. We sequenced soil floor and cow dung samples from households in Sirajganj district, Bangladesh, and identified potential pathogens and antibiotic resistance genes. We detected 182 potential pathogens in both soil and cow dung; organisms present in both sample types at the highest relative abundances were <i>Escherichia coli</i>, <i>Klebsiella pneumoniae, Salmonella enterica</i>, and <i>Pseudomonas aeruginosa</i>. Antibiotic resistance genes were found in all samples. In cow dung, the most common genes conferred resistance to the antibiotics lincosamide, rifamycin, cephamycin, tetracycline, and multiple antibiotics. In soil floors, the most common genes conferred resistance to rifamycin, sulfonamides, and multiple antibiotics. Household soil and cow dung may be important reservoirs of pathogens and antimicrobial resistance in low-income country settings with high levels of animal cohabitation compared to settings with finished household floors and minimal animal cohabitation.</p>\",\"PeriodicalId\":8002,\"journal\":{\"name\":\"Applied and Environmental Microbiology\",\"volume\":\" \",\"pages\":\"e0066925\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2025-06-18\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12175521/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Applied and Environmental Microbiology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/aem.00669-25\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/5/27 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q2\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.00669-25","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/5/27 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
Potential pathogens and antimicrobial resistance genes in household environments: a study of soil floors and cow dung in rural Bangladesh.
In low- and middle-income countries, living in homes with soil floors and animal cohabitation may expose children to fecal organisms, increasing the risk of enteric and antimicrobial-resistant infections. Our objective was to understand whether cow cohabitation in homes with soil floors in rural Bangladesh contributed to the presence and diversity of potential pathogens and antimicrobial resistance genes (ARGs) in the home. In 10 randomly selected households in rural Sirajganj District, we sampled floor soil and cow dung, which is commonly used as sealant in soil floors. We extracted DNA and performed shotgun metagenomic sequencing to explore potential pathogens and ARGs in each sample type. We detected 7 potential pathogens in soil only, 38 pathogens in cow dung only, and 182 pathogens in both soil and cow dung. Cow dung exhibited modestly higher potential pathogen genus richness compared to soil floors (Wilcoxon signed-rank test, P = 0.002). Using Bray-Curtis dissimilarity, potential pathogen species community composition differed between floors and cow dung (permutational multivariate analysis of variance, P < 0.001). All soil floor and cow dung samples contained ARGs; detected ARGs confer resistance to antibiotic classes including sulfonamides, rifamycin, aminoglycosides, lincosamides, and tetracycline. Paired floor and cow dung samples shared ARGs against rifamycin and glycopeptides, but otherwise, there was little overlap in resistomes between sample types. Our findings contribute to the growing literature on household soil and domestic animals as potentially important contributors to disease transmission and as reservoirs of antimicrobial resistance in low-income country settings.IMPORTANCEIn low-income countries, inadequate housing materials and animal cohabitation can lead to fecal contamination of rural homes. Contaminated soil floors are difficult to clean and may harbor organisms causing illness and antibiotic resistance, especially in young children, who frequently ingest soil. We sequenced soil floor and cow dung samples from households in Sirajganj district, Bangladesh, and identified potential pathogens and antibiotic resistance genes. We detected 182 potential pathogens in both soil and cow dung; organisms present in both sample types at the highest relative abundances were Escherichia coli, Klebsiella pneumoniae, Salmonella enterica, and Pseudomonas aeruginosa. Antibiotic resistance genes were found in all samples. In cow dung, the most common genes conferred resistance to the antibiotics lincosamide, rifamycin, cephamycin, tetracycline, and multiple antibiotics. In soil floors, the most common genes conferred resistance to rifamycin, sulfonamides, and multiple antibiotics. Household soil and cow dung may be important reservoirs of pathogens and antimicrobial resistance in low-income country settings with high levels of animal cohabitation compared to settings with finished household floors and minimal animal cohabitation.
期刊介绍:
Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.