Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment

April Z. Gu; Tianyu Cen; Xiangyang Li; Miao He; Dan Li; Jianmin Chen

doi:10.1016/j.envpol.2018.01.032

journal article Open Access Jun 01, 2018

Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment

April Z. Gu

Tianyu Cen Xiangyang Li

Miao He

Dan Li

Jianmin Chen

Environmental Pollution Vol. 237 pp. 74-82 · Elsevier BV

View at Publisher Save 10.1016/j.envpol.2018.01.032

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References

52

[1]

Call of the wild: antibiotic resistance genes in natural environments

Heather K. Allen, Justin Donato, Helena Huimi Wang et al.

Nature Reviews Microbiology 2010 10.1038/nrmicro2312

[2]

Anand "Role of some trace metal ions in placental membrane lipid peroxidation" Biol. Trace Elem. Res. (2001) 10.1385/bter:82:1-3:061

[3]

Microbiological effects of sublethal levels of antibiotics

Dan I. Andersson, Diarmaid Hughes

Nature Reviews Microbiology 2014 10.1038/nrmicro3270

[4]

Asakura "Genotoxicity studies of heavy metals: lead, bismuth, indium, silver and antimony" J. Occup. Health (2009) 10.1539/joh.l9080

[5]

Ashbolt "Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance" Environ. Health Perspect. (2013) 10.1289/ehp.1206316

[6]

Baharoglu "RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae" PLoS Genet. (2013) 10.1371/journal.pgen.1003421

[7]

Baker-Austin "Co-selection of antibiotic and metal resistance" Trends Microbiol. (2006) 10.1016/j.tim.2006.02.006

[8]

Beaber "SOS response promotes horizontal dissemination of antibiotic resistance genes" Nature (2004) 10.1038/nature02241

[9]

Berendonk "Tackling antibiotic resistance: the environmental framework" Nat. Rev. Microbiol. (2015) 10.1038/nrmicro3439

[10]

Breton "Ecotoxicology inside the gut: impact of heavy metals on the mouse microbiome" BMC Pharmacol. Toxicol. (2013) 10.1186/2050-6511-14-62

[11]

Cabral "Anthropogenic impact on mangrove sediments triggers differential responses in the heavy metals and antibiotic resistomes of microbial communities" Environ. Pollut. (2016) 10.1016/j.envpol.2016.05.078

[12]

Chen "Regulation of arsenite oxidation by the phosphate two-component system PhoBR in Halomonas sp. HAL1" Front. Microbiol. (2015) 10.3389/fmicb.2015.00923

[13]

Clinical and Laboratory Standards Institute (CLSI) (2012)

[14]

Outer membrane permeability and antibiotic resistance

Anne H. Delcour

Biochimica et Biophysica Acta (BBA) - Proteins and... 2009 10.1016/j.bbapap.2008.11.005

[15]

Ding "Enhanced uptake of antibiotic resistance genes in the presence of nanoalumina" Nanotoxicology (2016) 10.3109/17435390.2016.1161856

[16]

Furuya "Initiation and termination of DNA transfer during conjugation of IncI1 plasmid R64: roles of two sets of inverted repeat sequences within oriT in termination of R64 transfer" J. Bacteriol. (2000) 10.1128/jb.182.11.3191-3196.2000

[17]

Guo "Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater" Environ. Sci. Technol. (2015) 10.1021/acs.est.5b00644

[18]

He "Discharge of swine wastes risks water quality and food safety: antibiotics and antibiotic resistance genes from swine sources to the receiving environments" Environ. Int. (2016) 10.1016/j.envint.2016.03.023

[19]

Huang "Monitoring and evaluation of antibiotic-resistant bacteria at a municipal wastewater treatment plant in China" Environ. Int. (2012) 10.1016/j.envint.2011.03.001

[20]

Kabir "Investigation into the effect of soxR and soxS genes deletion on the central metabolism of Escherichia coli based on gene expressions and enzyme activities" Biochem. Eng. J. (2006) 10.1016/j.bej.2006.01.015

[21]

Kostelidou "Conserved C-terminal region of global repressor KorA of broad-host-range plasmid RK2 is required for co-operativity between KorA and a second RK2 global regulator, KorB" J. Mol. Biol. (1999) 10.1006/jmbi.1999.2761

[22]

Lebreton "AsrR is an oxidative stress sensing regulator modulating Enterococcus faecium opportunistic traits, antimicrobial resistance, and pathogenicity" PLoS Pathog. (2012) 10.1371/journal.ppat.1002834

[23]

Antimicrobial activity of metals: mechanisms, molecular targets and applications

Joseph A. Lemire, Joe J. Harrison, Raymond J. Turner

Nature Reviews Microbiology 2013 10.1038/nrmicro3028

[24]

Levy "Antibacterial resistance worldwide: causes, challenges and responses" Nat. Med. (2004) 10.1038/nm1145

[25]

Li "Water disinfection byproducts induce antibiotic resistance-role of environmental pollutants in resistance phenomena" Environ. Sci. Technol. (2016) 10.1021/acs.est.5b05113

[26]

Lv "Induction of bacterial antibiotic resistance by mutagenic halogenated nitrogenous disinfection byproducts" Environ. Pollut. (2015) 10.1016/j.envpol.2015.06.026

[27]

Martinez "What is a resistance gene? Ranking risk in resistomes" Nat. Rev. Microbiol. (2015) 10.1038/nrmicro3399

[28]

Martinez "Horizontal gene transfer of P-IB-type ATPases among bacteria isolated from radionuclide- and metal-contaminated subsurface soils" Appl. Environ. Microbiol. (2006) 10.1128/aem.72.5.3111-3118.2006

[29]

Mermod "The copper-inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli" Biometals (2012) 10.1007/s10534-011-9510-x

[30]

Ministry of Health, People's Republic of China. Environmental quality standard for soils (GB15618–2008).

[31]

Ministry of Health, People's Republic of China. Environmental quality standard for surface water (GB3838–2002).

[32]

Microbial heavy-metal resistance

D. H. Nies

Applied Microbiology and Biotechnology 1999 10.1007/s002530051457

[33]

Otto "Effects of antibacterial mineral leachates on the cellular ultrastructure, morphology, and membrane integrity of Escherichia coli and methicillin-resistant Staphylococcus aureus" Ann. Clin. Microbiol. Antimicrob. (2010) 10.1186/1476-0711-9-26

[34]

The Antioxidant Properties of Zinc

Saul R. Powell

The Journal of Nutrition 2000 10.1093/jn/130.5.1447s

[35]

Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera

Zhigang Qiu, Yunmei Yu, Zhaoli Chen et al.

Proceedings of the National Academy of Sciences 2012 10.1073/pnas.1107254109

[36]

Rodríguez Martín "Impact of 70 years urban growth associated with heavy metal pollution" Environ. Pollut. (2015) 10.1016/j.envpol.2014.10.014

[37]

Samuels "Conjugative junctions in RP4-mediated mating of Escherichia coli" J. Bacteriol. (2000) 10.1128/jb.182.10.2709-2715.2000

[38]

Schröder "Primary structure analysis and adhesion studies on the major outer membrane protein of Campylobacter jejuni" FEMS Microbiol. Lett. (1997) 10.1016/s0378-1097(97)00111-0

[39]

Seiler "Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture" Front. Microbiol. (2012) 10.3389/fmicb.2012.00399

[40]

Genome-wide Reconstruction of OxyR and SoxRS Transcriptional Regulatory Networks under Oxidative Stress in Escherichia coli K-12 MG1655

Sang Woo Seo, Donghyuk Kim, Richard Szubin et al.

Cell Reports 2015 10.1016/j.celrep.2015.07.043

[41]

Stepanauskas "Coselection for microbial resistance to metals and antibiotics in freshwater microcosms" Environ. Microbiol. (2006) 10.1111/j.1462-2920.2006.01091.x

[42]

Suzuki "Vanadium accelerates horizontal transfer of tet(M) gene from marine Photobacterium to Escherichia coli" FEMS Microbiol. Lett. (2012) 10.1111/j.1574-6968.2012.02653.x

[43]

Teng "Soil and soil environmental quality monitoring in China: a review" Environ. Int. (2014) 10.1016/j.envint.2014.04.014

[44]

United States Environmental Protection Agency (USEPA) (2009)

[45]

Wang "Ionic liquid facilitates the conjugative transfer of antibiotic resistance genes mediated by plasmid RP4" Environ. Sci. Technol. (2015) 10.1021/acs.est.5b01129

[46]

Wang "Triple functional DNA–protein conjugates: signal probes for Pb2+, using evanescent wave-induced emission" Biosens. Bioelectron. (2015) 10.1016/j.bios.2015.06.003

[47]

Waseem "Pollution status of Pakistan: a retrospective review on heavy metal contamination of water, soil, and vegetables" BioMed Res. Int. (2014) 10.1155/2014/813206

[48]

World Health Organization (WHO) (2011)

[49]

Zatyka "Cooperativity between KorB and TrbA repressors of broad-host-range plasmid RK2" J. Bacteriol. (2001) 10.1128/jb.183.3.1022-1031.2001

[50]

Zhang "Label-free colorimetric detection of Cu2+, on the basis of fenton reaction-assisted signal amplification with unmodified gold nanoparticles as indicator" Sensor. Actuator. B Chem. (2015) 10.1016/j.snb.2015.03.062

Showing 50 of 52 references

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References

Details

Published: Jun 01, 2018
Vol/Issue: 237
Pages: 74-82
License: View

Authors

A

April Z. Gu

School of Civil and Environmental Engineering, Cornell University, Ithaca, New York 14853, United States

College of Pharmaceutical Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P. R. China

J

Jianmin Chen

Shanghai Key Laboratory of Atmospheric Particle Pollution and Prevention, Department of Environmental Science and Engineering, Fudan University, Shanghai 200433, China; Shanghai Institute of Eco-Chongming (SIEC), No. 3663 Northern Zhongshan Road, Shanghai 200062, China

Funding

National Institute of Environmental Health Sciences Award: 3P42ES017109-07

Environmental Protection Agency Award: 83615501

United States National Science Foundation Award: CBET-1437257

China National Natural Science Foundation Award: 91643106

Cite This Article

April Z. Gu, Tianyu Cen, Xiangyang Li, et al. (2018). Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment. Environmental Pollution, 237, 74-82. https://doi.org/10.1016/j.envpol.2018.01.032

Sub-inhibitory concentrations of heavy metals facilitate the horizontal transfer of plasmid-mediated antibiotic resistance genes in water environment

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