Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern

Over the last few years, the cumulative use of antibiotics in healthcare institutions, as well as the rearing of livestock and poultry, has resulted in the accumulation of antibiotic resistance genes (ARGs). This presents a substantial danger to human health worldwide. The characteristics of airborn...

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Main Authors: Chang Zhao, Xinxin Liu, Haoxin Tan, Yucheng Bian, Muhammad Khalid, Aki Sinkkonen, Ari Jumpponen, Saeed ur Rahman, Baoming Du, Nan Hui
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412024001314
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author Chang Zhao
Xinxin Liu
Haoxin Tan
Yucheng Bian
Muhammad Khalid
Aki Sinkkonen
Ari Jumpponen
Saeed ur Rahman
Baoming Du
Nan Hui
author_facet Chang Zhao
Xinxin Liu
Haoxin Tan
Yucheng Bian
Muhammad Khalid
Aki Sinkkonen
Ari Jumpponen
Saeed ur Rahman
Baoming Du
Nan Hui
author_sort Chang Zhao
collection DOAJ
description Over the last few years, the cumulative use of antibiotics in healthcare institutions, as well as the rearing of livestock and poultry, has resulted in the accumulation of antibiotic resistance genes (ARGs). This presents a substantial danger to human health worldwide. The characteristics of airborne ARGs, especially those transferred from outdoors to indoors, remains largely unexplored in neighborhoods, even though a majority of human population spends most of their time there. We investigated airborne ARGs and mobile genetic element (MGE, IntI1), plant communities, and airborne microbiota transferred indoors, as well as respiratory disease (RD) prevalence using a combination of metabarcode sequencing, real-time quantitative PCR and questionnaires in 72 neighborhoods in Shanghai. We hypothesized that (i) urbanization regulates ARGs abundance, (ii) the urbanization effect on ARGs varies seasonally, and (iii) land use types are associated with ARGs abundance. Supporting these hypotheses, during the warm season, the abundance of ARGs in peri-urban areas was higher than in urban areas. The abundance of ARGs was also affected by the surrounding land use and plant communities: an increase in the proportion of gray infrastructure (e.g., residential area) around neighborhoods can lead to an increase in some ARGs (mecA, qnrA, ermB and mexD). Additionally, there were variations observed in the relationship between ARGs and bacterial genera in different seasons. Specifically, Stenotrophomonas and Campylobacter were positively correlated with vanA during warm seasons, whereas Pseudomonas, Bacteroides, Treponema and Stenotrophomonas positively correlated with tetX in the cold season. Interstingly, a noteworthy positive correlation was observed between the abundance of vanA and the occurrence of both rhinitis and rhinoconjunctivitis. Taken together, our study underlines the importance of urbanization and season in controlling the indoor transfer of airborne ARGs. Furthermore, we also highlight the augmentation of green–blue infrastructure in urban environments has the potential to mitigate an excess of ARGs.
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spelling doaj.art-0c05a00d2d4c45ada9fcd5c5672597312024-03-23T06:22:18ZengElsevierEnvironment International0160-41202024-03-01185108545Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent patternChang Zhao0Xinxin Liu1Haoxin Tan2Yucheng Bian3Muhammad Khalid4Aki Sinkkonen5Ari Jumpponen6Saeed ur Rahman7Baoming Du8Nan Hui9School of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, China; Shanghai Yangtze River Delta Eco-Environmental Change and Management Observation and Research Station, Ministry of Science and Technology, Ministry of Education, 800 Dongchuan Rd, 200240, Shanghai, China; Shanghai Urban Forest Ecosystem Research Station, National Forestry and Grassland Administration, 800 Dongchuan Rd., 200240, Shanghai, ChinaSchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, China; Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, Lahti 15140 FinlandSchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, ChinaSchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, ChinaDepartment of Biology, College of Science and Technology, Wenzhou-Kean University, Wenzhou, ChinaFaculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, Lahti 15140 Finland; Horticulture Technologies, Unit of Production Systems, Natural Resources Institute Finland, Turku, FinlandDivision of Biology, Kansas State University, Manhattan, KS, USASchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, ChinaSchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, ChinaSchool of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd., 200240, Shanghai, China; Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, Lahti 15140 Finland; Corresponding author.Over the last few years, the cumulative use of antibiotics in healthcare institutions, as well as the rearing of livestock and poultry, has resulted in the accumulation of antibiotic resistance genes (ARGs). This presents a substantial danger to human health worldwide. The characteristics of airborne ARGs, especially those transferred from outdoors to indoors, remains largely unexplored in neighborhoods, even though a majority of human population spends most of their time there. We investigated airborne ARGs and mobile genetic element (MGE, IntI1), plant communities, and airborne microbiota transferred indoors, as well as respiratory disease (RD) prevalence using a combination of metabarcode sequencing, real-time quantitative PCR and questionnaires in 72 neighborhoods in Shanghai. We hypothesized that (i) urbanization regulates ARGs abundance, (ii) the urbanization effect on ARGs varies seasonally, and (iii) land use types are associated with ARGs abundance. Supporting these hypotheses, during the warm season, the abundance of ARGs in peri-urban areas was higher than in urban areas. The abundance of ARGs was also affected by the surrounding land use and plant communities: an increase in the proportion of gray infrastructure (e.g., residential area) around neighborhoods can lead to an increase in some ARGs (mecA, qnrA, ermB and mexD). Additionally, there were variations observed in the relationship between ARGs and bacterial genera in different seasons. Specifically, Stenotrophomonas and Campylobacter were positively correlated with vanA during warm seasons, whereas Pseudomonas, Bacteroides, Treponema and Stenotrophomonas positively correlated with tetX in the cold season. Interstingly, a noteworthy positive correlation was observed between the abundance of vanA and the occurrence of both rhinitis and rhinoconjunctivitis. Taken together, our study underlines the importance of urbanization and season in controlling the indoor transfer of airborne ARGs. Furthermore, we also highlight the augmentation of green–blue infrastructure in urban environments has the potential to mitigate an excess of ARGs.http://www.sciencedirect.com/science/article/pii/S0160412024001314Neighborhoodsairborne ARGs transferred indoorsUrbanizationSeasonRespiratory diseases
spellingShingle Chang Zhao
Xinxin Liu
Haoxin Tan
Yucheng Bian
Muhammad Khalid
Aki Sinkkonen
Ari Jumpponen
Saeed ur Rahman
Baoming Du
Nan Hui
Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
Environment International
Neighborhoods
airborne ARGs transferred indoors
Urbanization
Season
Respiratory diseases
title Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
title_full Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
title_fullStr Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
title_full_unstemmed Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
title_short Urbanization influences the indoor transfer of airborne antibiotic resistance genes, which has a seasonally dependent pattern
title_sort urbanization influences the indoor transfer of airborne antibiotic resistance genes which has a seasonally dependent pattern
topic Neighborhoods
airborne ARGs transferred indoors
Urbanization
Season
Respiratory diseases
url http://www.sciencedirect.com/science/article/pii/S0160412024001314
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