The Composition and Spatial Patterns of Bacterial Virulence Factors and Antibiotic Resistance Genes in 19 Wastewater Treatment Plants
Abstract
Bacterial pathogenicity and antibiotic resistance are of concern for environmental safety and public health. Accumulating evidence suggests that wastewater treatment plants (WWTPs) are as an important sink and source of pathogens and antibiotic resistance genes (ARGs). Virulence genes (encoding virulence factors) are good indicators for bacterial pathogenic potentials. To achieve a comprehensive understanding of bacterial pathogenic potentials and antibiotic resistance in WWTPs, bacterial virulence genes and ARGs in 19 WWTPs covering a majority of latitudinal zones of China were surveyed by using GeoChip 4.2. A total of 1610 genes covering 13 virulence factors and 1903 genes belonging to 11 ARG families were detected respectively. The bacterial virulence genes exhibited significant spatial distribution patterns of a latitudinal biodiversity gradient and a distance-decay relationship across China. Moreover, virulence genes tended to coexist with ARGs as shown by their strongly positive associations. In addition, key environmental factors shaping the overall virulence gene structure were identified. This study profiles the occurrence, composition and distribution of virulence genes and ARGs in current WWTPs in China, and uncovers spatial patterns and important environmental variables shaping their structure, which may provide the basis for further studies of bacterial virulence factors and antibiotic resistance in WWTPs.
- Authors:
-
- Tsinghua Univ., Beijing (China). School of Environment. Environmental Simulation and Pollution Control State Key
- Tsinghua Univ., Beijing (China). School of Environment. Environmental Simulation and Pollution Control State Key; Univ. of Oklahoma, Norman, OK (United States). Dept. of Microbiology and Plant Biology and School of Civil Engineering and Environmental Sciences; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth Sciences Division; Chinese Academy of Sciences (CAS), Beijing (China).
- Chinese Academy of Sciences (CAS), Beijing (China). Research Center for Eco-environmental Sciences. State Key Lab. of Environmental Aquatic Chemistry
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1627807
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics
Citation Formats
Zhang, Bing, Xia, Yu, Wen, Xianghua, Wang, Xiaohui, Yang, Yunfeng, Zhou, Jizhong, and Zhang, Yu. The Composition and Spatial Patterns of Bacterial Virulence Factors and Antibiotic Resistance Genes in 19 Wastewater Treatment Plants. United States: N. p., 2016.
Web. doi:10.1371/journal.pone.0167422.
Zhang, Bing, Xia, Yu, Wen, Xianghua, Wang, Xiaohui, Yang, Yunfeng, Zhou, Jizhong, & Zhang, Yu. The Composition and Spatial Patterns of Bacterial Virulence Factors and Antibiotic Resistance Genes in 19 Wastewater Treatment Plants. United States. https://doi.org/10.1371/journal.pone.0167422
Zhang, Bing, Xia, Yu, Wen, Xianghua, Wang, Xiaohui, Yang, Yunfeng, Zhou, Jizhong, and Zhang, Yu. Thu .
"The Composition and Spatial Patterns of Bacterial Virulence Factors and Antibiotic Resistance Genes in 19 Wastewater Treatment Plants". United States. https://doi.org/10.1371/journal.pone.0167422. https://www.osti.gov/servlets/purl/1627807.
@article{osti_1627807,
title = {The Composition and Spatial Patterns of Bacterial Virulence Factors and Antibiotic Resistance Genes in 19 Wastewater Treatment Plants},
author = {Zhang, Bing and Xia, Yu and Wen, Xianghua and Wang, Xiaohui and Yang, Yunfeng and Zhou, Jizhong and Zhang, Yu},
abstractNote = {Bacterial pathogenicity and antibiotic resistance are of concern for environmental safety and public health. Accumulating evidence suggests that wastewater treatment plants (WWTPs) are as an important sink and source of pathogens and antibiotic resistance genes (ARGs). Virulence genes (encoding virulence factors) are good indicators for bacterial pathogenic potentials. To achieve a comprehensive understanding of bacterial pathogenic potentials and antibiotic resistance in WWTPs, bacterial virulence genes and ARGs in 19 WWTPs covering a majority of latitudinal zones of China were surveyed by using GeoChip 4.2. A total of 1610 genes covering 13 virulence factors and 1903 genes belonging to 11 ARG families were detected respectively. The bacterial virulence genes exhibited significant spatial distribution patterns of a latitudinal biodiversity gradient and a distance-decay relationship across China. Moreover, virulence genes tended to coexist with ARGs as shown by their strongly positive associations. In addition, key environmental factors shaping the overall virulence gene structure were identified. This study profiles the occurrence, composition and distribution of virulence genes and ARGs in current WWTPs in China, and uncovers spatial patterns and important environmental variables shaping their structure, which may provide the basis for further studies of bacterial virulence factors and antibiotic resistance in WWTPs.},
doi = {10.1371/journal.pone.0167422},
journal = {PLoS ONE},
number = 12,
volume = 11,
place = {United States},
year = {Thu Dec 01 00:00:00 EST 2016},
month = {Thu Dec 01 00:00:00 EST 2016}
}
Figures / Tables:
Works referenced in this record:
Siderophores: Structure and Function of Microbial Iron Transport Compounds
journal, November 1995
- Neilands, J. B.
- Journal of Biological Chemistry, Vol. 270, Issue 45
Antibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters
journal, March 2016
- Ju, Feng; Li, Bing; Ma, Liping
- Water Research, Vol. 91
DNA recovery from soils of diverse composition.
journal, January 1996
- Zhou, J.; Bruns, M. A.; Tiedje, J. M.
- Applied and environmental microbiology, Vol. 62, Issue 2
Latitudinal gradients in diversity: real patterns and random models
journal, June 2001
- Koleff, Patricia; Gaston, Kevin J.
- Ecography, Vol. 24, Issue 3
VFDB: a reference database for bacterial virulence factors
journal, December 2004
- Chen, L.
- Nucleic Acids Research, Vol. 33, Issue Database issue
Antibiotic resistance in the environment: a link to the clinic?
journal, October 2010
- Wright, Gerard D.
- Current Opinion in Microbiology, Vol. 13, Issue 5
Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake
journal, March 2014
- Czekalski, Nadine; Gascón Díez, Elena; Bürgmann, Helmut
- The ISME Journal, Vol. 8, Issue 7
Functional gene diversity of soil microbial communities from five oil-contaminated fields in China
journal, September 2010
- Liang, Yuting; Van Nostrand, Joy D.; Deng, Ye
- The ISME Journal, Vol. 5, Issue 3
Common themes in microbial pathogenicity revisited.
journal, January 1997
- Finlay, B. B.; Falkow, S.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 2
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007
- He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
- The ISME Journal, Vol. 1, Issue 1
Molecular mechanisms of antibiotic resistance
journal, December 2014
- Blair, Jessica M. A.; Webber, Mark A.; Baylay, Alison J.
- Nature Reviews Microbiology, Vol. 13, Issue 1
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats
journal, January 2015
- Zhou, Jizhong; He, Zhili; Yang, Yunfeng
- mBio, Vol. 6, Issue 1
Discovery of virulence factors of pathogenic bacteria
journal, February 2008
- Wu, Hsing-Ju; Wang, Andrew H-J; Jennings, Michael P.
- Current Opinion in Chemical Biology, Vol. 12, Issue 1
Processes controlling the transmission of bacterial pathogens in the environment
journal, April 2007
- Yildiz, Fitnat H.
- Research in Microbiology, Vol. 158, Issue 3
Functional ecology of an Antarctic Dry Valley
journal, May 2013
- Chan, Y.; Van Nostrand, J. D.; Zhou, J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics
journal, January 2015
- Berglund, Björn
- Infection Ecology & Epidemiology, Vol. 5, Issue 1
A meta-analysis of changes in bacterial and archaeal communities with time
journal, April 2013
- Shade, Ashley; Gregory Caporaso, J.; Handelsman, Jo
- The ISME Journal, Vol. 7, Issue 8
The microbial gene diversity along an elevation gradient of the Tibetan grassland
journal, August 2013
- Yang, Yunfeng; Gao, Ying; Wang, Shiping
- The ISME Journal, Vol. 8, Issue 2
Determination of antibiotic substances in hospital sewage water using solid phase extraction and liquid chromatography/mass spectrometry and group analogue internal standards
journal, December 2004
- Lindberg, Richard; Jarnheimer, Per-Åke; Olsen, Björn
- Chemosphere, Vol. 57, Issue 10
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
journal, April 2014
- Zhao, Mengxin; Xue, Kai; Wang, Feng
- The ISME Journal, Vol. 8, Issue 10
Detection of bacterial pathogens in municipal wastewater using an oligonucleotide microarray and real-time quantitative PCR
journal, June 2006
- Lee, Dae-Young; Shannon, Kelly; Beaudette, Lee A.
- Journal of Microbiological Methods, Vol. 65, Issue 3
GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity
journal, April 2010
- He, Zhili; Deng, Ye; Van Nostrand, Joy D.
- The ISME Journal, Vol. 4, Issue 9
Antibiotics and Antibiotic Resistance Genes in Natural Environments
journal, July 2008
- Martinez, J. L.
- Science, Vol. 321, Issue 5887
Recent Advances in Multi-Drug Resistance (MDR) Efflux Pump Inhibitors of Gram-Positive Bacteria S. aureus
journal, February 2013
- Handzlik, Jadwiga; Matys, Anna; Kieć-Kononowicz, Katarzyna
- Antibiotics, Vol. 2, Issue 1
High Temperature and Bacteriophages Can Indirectly Select for Bacterial Pathogenicity in Environmental Reservoirs
journal, March 2011
- Friman, Ville-Petri; Hiltunen, Teppo; Jalasvuori, Matti
- PLoS ONE, Vol. 6, Issue 3
Inactivation of antibiotics and the dissemination of resistance genes
journal, April 1994
- Davies, J.
- Science, Vol. 264, Issue 5157
Molecular evolution and the latitudinal biodiversity gradient
journal, March 2013
- Dowle, E. J.; Morgan-Richards, M.; Trewick, S. A.
- Heredity, Vol. 110, Issue 6
Spatial scaling of functional gene diversity across various microbial taxa
journal, May 2008
- Zhou, J.; Kang, S.; Schadt, C. W.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 22
Development of functional gene microarrays for microbial community analysis
journal, February 2012
- He, Zhili; Deng, Ye; Zhou, Jizhong
- Current Opinion in Biotechnology, Vol. 23, Issue 1
Exploring Variation of Antibiotic Resistance Genes in Activated Sludge over a Four-Year Period through a Metagenomic Approach
journal, August 2013
- Yang, Ying; Li, Bing; Ju, Feng
- Environmental Science & Technology, Vol. 47, Issue 18
Antimicrobial resistance of integron-harboring Escherichia coli isolates from clinical samples, wastewater treatment plant and river water
journal, January 2012
- Koczura, Ryszard; Mokracka, Joanna; Jabłońska, Lucyna
- Science of The Total Environment, Vol. 414
Community analysis of ammonia-oxidizing bacteria in activated sludge of eight wastewater treatment systems
journal, January 2010
- Wang, Xiaohui; Wen, Xianghua; Criddle, Craig
- Journal of Environmental Sciences, Vol. 22, Issue 4
Insight into the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to antimicrobial drugs analysed by the 454-pyrosequencing technology
journal, August 2008
- Szczepanowski, Rafael; Bekel, Thomas; Goesmann, Alexander
- Journal of Biotechnology, Vol. 136, Issue 1-2
Occurrence, Abundance, and Diversity of Tetracycline Resistance Genes in 15 Sewage Treatment Plants across China and Other Global Locations
journal, April 2011
- Zhang, Xu-Xiang; Zhang, Tong
- Environmental Science & Technology, Vol. 45, Issue 7
Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach
journal, May 2015
- Zhang, Tong; Yang, Ying; Pruden, Amy
- Applied Microbiology and Biotechnology, Vol. 99, Issue 18
Microbial community functional structure in response to antibiotics in pharmaceutical wastewater treatment systems
journal, October 2013
- Zhang, Yu; Xie, Jianping; Liu, Miaomiao
- Water Research, Vol. 47, Issue 16
The PathoChip, a functional gene array for assessing pathogenic properties of diverse microbial communities
journal, June 2013
- Lee, Yong-Jin; van Nostrand, Joy D.; Tu, Qichao
- The ISME Journal, Vol. 7, Issue 10
Bacterial multidrug efflux pumps: Mechanisms, physiology and pharmacological exploitations
journal, October 2014
- Sun, Jingjing; Deng, Ziqing; Yan, Aixin
- Biochemical and Biophysical Research Communications, Vol. 453, Issue 2
Antibiotic resistance genes in water environment
journal, March 2009
- Zhang, Xu-Xiang; Zhang, Tong; Fang, Herbert H. P.
- Applied Microbiology and Biotechnology, Vol. 82, Issue 3
The Microbiomes in Lichen and Moss Biocrust Contribute Differently to Carbon and Nitrogen Cycles in Arid Ecosystems
journal, July 2022
- Tian, Chang; Pang, Jingwen; Bu, Chongfeng
- Microbial Ecology, Vol. 86, Issue 1
Effect of temperature on removal of antibiotic resistance genes by anaerobic digestion of activated sludge revealed by metagenomic approach
journal, May 2015
- Zhang, Tong; Yang, Ying; Pruden, Amy
- Applied Microbiology and Biotechnology, Vol. 99, Issue 18
Distribution of pharmaceutical and personal care products (PPCPs) in aquatic environment in Hanoi and Metro Manila
journal, November 2021
- Van, Dieu-Anh; Ngo, Thanh Huy; Huynh, Trung Hai
- Environmental Monitoring and Assessment, Vol. 193, Issue 12
Development of functional gene microarrays for microbial community analysis
journal, February 2012
- He, Zhili; Deng, Ye; Zhou, Jizhong
- Current Opinion in Biotechnology, Vol. 23, Issue 1
Insight into the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to antimicrobial drugs analysed by the 454-pyrosequencing technology
journal, August 2008
- Szczepanowski, Rafael; Bekel, Thomas; Goesmann, Alexander
- Journal of Biotechnology, Vol. 136, Issue 1-2
Detection of bacterial pathogens in municipal wastewater using an oligonucleotide microarray and real-time quantitative PCR
journal, June 2006
- Lee, Dae-Young; Shannon, Kelly; Beaudette, Lee A.
- Journal of Microbiological Methods, Vol. 65, Issue 3
Microbial community functional structure in response to antibiotics in pharmaceutical wastewater treatment systems
journal, October 2013
- Zhang, Yu; Xie, Jianping; Liu, Miaomiao
- Water Research, Vol. 47, Issue 16
Antibiotic resistance genes and human bacterial pathogens: Co-occurrence, removal, and enrichment in municipal sewage sludge digesters
journal, March 2016
- Ju, Feng; Li, Bing; Ma, Liping
- Water Research, Vol. 91
Temperature-regulated expression of bacterial virulence genes
journal, February 2000
- Konkel, Michael E.; Tilly, Kit
- Microbes and Infection, Vol. 2, Issue 2
Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations
journal, December 2003
- Russell, Ad
- The Lancet Infectious Diseases, Vol. 3, Issue 12
Occurrence, Abundance, and Diversity of Tetracycline Resistance Genes in 15 Sewage Treatment Plants across China and Other Global Locations
journal, April 2011
- Zhang, Xu-Xiang; Zhang, Tong
- Environmental Science & Technology, Vol. 45, Issue 7
Exploring Variation of Antibiotic Resistance Genes in Activated Sludge over a Four-Year Period through a Metagenomic Approach
journal, August 2013
- Yang, Ying; Li, Bing; Ju, Feng
- Environmental Science & Technology, Vol. 47, Issue 18
Molecular evolution and the latitudinal biodiversity gradient
journal, March 2013
- Dowle, E. J.; Morgan-Richards, M.; Trewick, S. A.
- Heredity, Vol. 110, Issue 6
GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes
journal, May 2007
- He, Zhili; Gentry, Terry J.; Schadt, Christopher W.
- The ISME Journal, Vol. 1, Issue 1
Functional gene diversity of soil microbial communities from five oil-contaminated fields in China
journal, September 2010
- Liang, Yuting; Van Nostrand, Joy D.; Deng, Ye
- The ISME Journal, Vol. 5, Issue 3
A meta-analysis of changes in bacterial and archaeal communities with time
journal, April 2013
- Shade, Ashley; Gregory Caporaso, J.; Handelsman, Jo
- The ISME Journal, Vol. 7, Issue 8
Microbial mediation of biogeochemical cycles revealed by simulation of global changes with soil transplant and cropping
journal, April 2014
- Zhao, Mengxin; Xue, Kai; Wang, Feng
- The ISME Journal, Vol. 8, Issue 10
Molecular mechanisms of antibiotic resistance
journal, December 2014
- Blair, Jessica M. A.; Webber, Mark A.; Baylay, Alison J.
- Nature Reviews Microbiology, Vol. 13, Issue 1
Functional ecology of an Antarctic Dry Valley
journal, May 2013
- Chan, Y.; Van Nostrand, J. D.; Zhou, J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 22
VFDB: a reference database for bacterial virulence factors
journal, December 2004
- Chen, L.
- Nucleic Acids Research, Vol. 33, Issue Database issue
GeoChip 4: a functional gene-array-based high-throughput environmental technology for microbial community analysis
journal, March 2014
- Tu, Qichao; Yu, Hao; He, Zhili
- Molecular Ecology Resources
Latitudinal gradients in diversity: real patterns and random models
journal, June 2001
- Koleff, Patricia; Gaston, Kevin J.
- Ecography, Vol. 24, Issue 3
Inactivation of antibiotics and the dissemination of resistance genes
journal, April 1994
- Davies, J.
- Science, Vol. 264, Issue 5157
In Situ-Synthesized Virulence and Marker Gene Biochip for Detection of Bacterial Pathogens in Water
journal, February 2008
- Miller, S. M.; Tourlousse, D. M.; Stedtfeld, R. D.
- Applied and Environmental Microbiology, Vol. 74, Issue 7
Comparison of the Microbial Community Structures of Untreated Wastewaters from Different Geographic Locales
journal, February 2013
- Shanks, Orin C.; Newton, Ryan J.; Kelty, Catherine A.
- Applied and Environmental Microbiology, Vol. 79, Issue 9
Common themes in microbial pathogenicity revisited
journal, June 1997
- Finlay, B. B.; Falkow, S.
- Microbiology and Molecular Biology Reviews, Vol. 61, Issue 2
Environmental dissemination of antibiotic resistance genes and correlation to anthropogenic contamination with antibiotics
journal, January 2015
- Berglund, Björn
- Infection Ecology & Epidemiology, Vol. 5, Issue 1
Works referencing / citing this record:
Virulence factor activity relationships (VFARs): a bioinformatics perspective
journal, January 2017
- Waseem, Hassan; Williams, Maggie R.; Stedtfeld, Tiffany
- Environmental Science: Processes & Impacts, Vol. 19, Issue 3
A Metagenomic Approach to Evaluating Surface Water Quality in Haiti
journal, October 2018
- Roy, Monika; Arnaud, Jean; Jasmin, Paul
- International Journal of Environmental Research and Public Health, Vol. 15, Issue 10
Research and Technological Advances Regarding the Study of the Spread of Antimicrobial Resistance Genes and Antimicrobial-Resistant Bacteria Related to Animal Husbandry
journal, December 2019
- Li, Na; Liu, Chong; Zhang, Zhiguo
- International Journal of Environmental Research and Public Health, Vol. 16, Issue 24
Figures / Tables found in this record: