Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters
ABSTRACT Antimicrobial resistance (AMR) seriously threatens public health by reducing antibiotic effectiveness in curing bacterial infections. Atmospheric particulate matter (APM) is a common environmental hazard that affects human health by causing various diseases and disseminating bacterial patho...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-10-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00698-22 |
| _version_ | 1811336175483355136 |
|---|---|
| author | Ziyun Li Mei Li Shuhui Tong Meng Fang Weiwei Li Ling Li Xiang Li Hai Xu Xiaomin Sun Mingyu Wang |
| author_facet | Ziyun Li Mei Li Shuhui Tong Meng Fang Weiwei Li Ling Li Xiang Li Hai Xu Xiaomin Sun Mingyu Wang |
| author_sort | Ziyun Li |
| collection | DOAJ |
| description | ABSTRACT Antimicrobial resistance (AMR) seriously threatens public health by reducing antibiotic effectiveness in curing bacterial infections. Atmospheric particulate matter (APM) is a common environmental hazard that affects human health by causing various diseases and disseminating bacterial pathogenesis, of which pathogenic bacteria and AMR are essential parts. The properties of APM microbiomes and resistomes, along with their shaping factors and mutual relationships, need further examination. To address this, we analyzed APMs collected from 13 cities within four clusters (North and South China, Inner Mongolia, and Tibet). Significant regionalization was found for both the microbiomes (P < 0.001) and core resistomes (P < 0.001) for APMs, with statistical analyses showing significant differences in different regions. Principal coordinate analysis (PCoA) and accompanying ANOSIM analyses showed that microbiomes and core resistomes followed the same regional subclustering hierarchy patterns. This finding, together with response analysis of APM microbiomes and core resistomes to environmental parameters that showed similar response patterns, as well as Procrustes analysis (M2 = 0.963, P < 0.05) between APM microbiomes and core resistomes, strongly suggested that APM microbiomes and core resistomes are correlated. Co-occurrence network analysis further revealed key taxa and antimicrobial resistance determinants in the interactions between APM microbiomes and core resistomes. Thus, it was concluded that APM microbiome and resistome compositions were highly regional, that environmental pollutants and APM levels impacted APM microbiomes and resistomes, and that microbiomes and resistomes in APMs are significantly correlated (P < 0.05). IMPORTANCE Bacteria associated with atmospheric particulate matter (APMs) can transmit over long distances. A large portion of these bacteria can potentially threaten human health. The antimicrobial resistance (AMR) of pathogenic bacteria carried by APMs prevents curing from infections. Therefore, both the pathogenic bacteria in APMs and their AMR are receiving more attention. The literature suggests a knowledge gap that exists for bacterial AMR and bacterial pathogenesis in APMs, including their distribution patterns, mutual relationships, and factors influencing their compositions. This work aimed to bridge this knowledge gap by studying APM samples collected from 13 cities. The results demonstrated that both bacteria and antibiotic resistance determinants were highly regional and that their composition patterns were significantly correlated, and influenced by the same group of environmental factors. This study thus determined the relationship between the two important aspects of bacterial pathogenesis in APMs and represents significant progress in understanding bacterial pathogenesis in APMs. |
| first_indexed | 2024-04-13T17:35:36Z |
| format | Article |
| id | doaj.art-f5a388e89f37423aaa1454eee54183d4 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-13T17:35:36Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-f5a388e89f37423aaa1454eee54183d42022-12-22T02:37:24ZengAmerican Society for MicrobiologymSystems2379-50772022-10-017510.1128/msystems.00698-22Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate MattersZiyun Li0Mei Li1Shuhui Tong2Meng Fang3Weiwei Li4Ling Li5Xiang Li6Hai Xu7Xiaomin Sun8Mingyu Wang9State Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaInstitute of Mass Spectrometer and Atmospheric Environment, Jinan University, Guangzhou, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaDepartment of Environmental Science and Engineering, Fudan University, Shanghai, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaEnvironment Research Institute, Shandong University, Qingdao, ChinaState Key Laboratory of Microbial Technology, Shandong University, Qingdao, ChinaABSTRACT Antimicrobial resistance (AMR) seriously threatens public health by reducing antibiotic effectiveness in curing bacterial infections. Atmospheric particulate matter (APM) is a common environmental hazard that affects human health by causing various diseases and disseminating bacterial pathogenesis, of which pathogenic bacteria and AMR are essential parts. The properties of APM microbiomes and resistomes, along with their shaping factors and mutual relationships, need further examination. To address this, we analyzed APMs collected from 13 cities within four clusters (North and South China, Inner Mongolia, and Tibet). Significant regionalization was found for both the microbiomes (P < 0.001) and core resistomes (P < 0.001) for APMs, with statistical analyses showing significant differences in different regions. Principal coordinate analysis (PCoA) and accompanying ANOSIM analyses showed that microbiomes and core resistomes followed the same regional subclustering hierarchy patterns. This finding, together with response analysis of APM microbiomes and core resistomes to environmental parameters that showed similar response patterns, as well as Procrustes analysis (M2 = 0.963, P < 0.05) between APM microbiomes and core resistomes, strongly suggested that APM microbiomes and core resistomes are correlated. Co-occurrence network analysis further revealed key taxa and antimicrobial resistance determinants in the interactions between APM microbiomes and core resistomes. Thus, it was concluded that APM microbiome and resistome compositions were highly regional, that environmental pollutants and APM levels impacted APM microbiomes and resistomes, and that microbiomes and resistomes in APMs are significantly correlated (P < 0.05). IMPORTANCE Bacteria associated with atmospheric particulate matter (APMs) can transmit over long distances. A large portion of these bacteria can potentially threaten human health. The antimicrobial resistance (AMR) of pathogenic bacteria carried by APMs prevents curing from infections. Therefore, both the pathogenic bacteria in APMs and their AMR are receiving more attention. The literature suggests a knowledge gap that exists for bacterial AMR and bacterial pathogenesis in APMs, including their distribution patterns, mutual relationships, and factors influencing their compositions. This work aimed to bridge this knowledge gap by studying APM samples collected from 13 cities. The results demonstrated that both bacteria and antibiotic resistance determinants were highly regional and that their composition patterns were significantly correlated, and influenced by the same group of environmental factors. This study thus determined the relationship between the two important aspects of bacterial pathogenesis in APMs and represents significant progress in understanding bacterial pathogenesis in APMs.https://journals.asm.org/doi/10.1128/msystems.00698-22antimicrobial resistanceatmospheric particulate matterbacterial pathogenesismicrobiomeresistomeshaping factors |
| spellingShingle | Ziyun Li Mei Li Shuhui Tong Meng Fang Weiwei Li Ling Li Xiang Li Hai Xu Xiaomin Sun Mingyu Wang Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters mSystems antimicrobial resistance atmospheric particulate matter bacterial pathogenesis microbiome resistome shaping factors |
| title | Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters |
| title_full | Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters |
| title_fullStr | Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters |
| title_full_unstemmed | Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters |
| title_short | Regionalization and Shaping Factors for Microbiomes and Core Resistomes in Atmospheric Particulate Matters |
| title_sort | regionalization and shaping factors for microbiomes and core resistomes in atmospheric particulate matters |
| topic | antimicrobial resistance atmospheric particulate matter bacterial pathogenesis microbiome resistome shaping factors |
| url | https://journals.asm.org/doi/10.1128/msystems.00698-22 |
| work_keys_str_mv | AT ziyunli regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT meili regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT shuhuitong regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT mengfang regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT weiweili regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT lingli regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT xiangli regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT haixu regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT xiaominsun regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters AT mingyuwang regionalizationandshapingfactorsformicrobiomesandcoreresistomesinatmosphericparticulatematters |