Insight into co-hosts of nitrate reduction genes and antibiotic resistance genes in an urban river of the qinghai-tibet plateau

Hu, Jinyun; Chen, Qian; Zhong, Sining; Liu, Yaping; Gao, Qiang; Graham, Emily B.; Chen, Huan; Sun, Weiling

doi:10.1016/j.watres.2022.119189

Title: Insight into co-hosts of nitrate reduction genes and antibiotic resistance genes in an urban river of the qinghai-tibet plateau

Journal Article · Fri Sep 30 00:00:00 EDT 2022 · Water Research

DOI:https://doi.org/10.1016/j.watres.2022.119189· OSTI ID:1895126

Hu, Jinyun ^[1]; Chen, Qian ^[1]; Zhong, Sining ^[2]; Liu, Yaping ^[1]; Gao, Qiang ^[3];

^[4];

^[5];

^[1]

Peking Univ., Beijing (China); State Environmental Protection Key Laboratory of All Material Fluxes in River Ecosystems, Beijing (China)
Fujian Agriculture and Forestry University, Fuzhou (China)
Qinghai University, Xining (China)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Washington State Univ., Richland, WA (United States)
Clemson Univ., SC (United States)

Microbial co-hosts of nitrate reduction genes (NRGs) and antibiotic resistance genes (ARGs) have been recently reported, but their ecology and biochemical role in urban waterways remain largely unknown. Here, we collected 69 surface water and sediment samples in the Huangshui River on the Qinghai-Tibet Plateau during the wet and dry season associated with comparatively low and high antibiotic levels. Using metagenomic sequencing, we retrieved 278 medium-to-high-quality metagenome-assembled genomes (MAGs) of NRG-ARG co-hosts, mainly belonging to the phyla Proteobacteria, Actinobacteriota, and Bacteroidota. Of microorganisms carrying ARGs, a high proportion (75.3?94.9%) also encoded NRGs, supporting nitrate reducing bacteria as dominant hosts of ARGs. Seasonal changes in antibiotic levels corresponded to significant variation in the relative abundance and community composition of NRG-ARG co-host in both water and sediments, resulting in a concomitant change in antibiotic resistance pathways. In contrast, the contribution of NRG-ARG co-hosts to nitrate reduction was stable between seasons. Further, we identify specific antibiotics (e.g., sulphonamides) and microbial taxa (e.g., Acinetobacter and Hafnia) that may disproportionately impact these relationships to serve as a basis for laboratory investigations into bioremediation strategies. Our study suggests that highly abundant nitrate reducing microorganisms in contaminated environments may also directly impact human health as carriers of antibiotic resistance.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE; National Natural Science Foundation of China (NSFC); Natural Science Foundation of Qinghai Province; USDA National Institute of Food and Agriculture (NIFA)

Grant/Contract Number:: AC05-76RL01830; 51925901; 52070002; 2019-ZJ-952Q

OSTI ID:: 1895126

Report Number(s):: PNNL-SA-172262

Journal Information:: Water Research, Vol. 225; ISSN 0043-1354

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Forecasting the dissemination of antibiotic resistance genes across bacterial genomes Ellabaan, Mostafa M. H.; Munck, Christian; Porse, Andreas Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-22757-1	journal	April 2021
Effects of amoxicillin on nitrogen transformation and bacterial community succession during aerobic composting Liu, Ning; Hou, Tao; Yin, Hongjie Journal of Hazardous Materials, Vol. 362 https://doi.org/10.1016/j.jhazmat.2018.09.028	journal	January 2019
Comammox Nitrospira within the Yangtze River continuum: community, biogeography, and ecological drivers Liu, Shufeng; Wang, Haiying; Chen, Liming The ISME Journal, Vol. 14, Issue 10 https://doi.org/10.1038/s41396-020-0701-8	journal	June 2020
STAMP: statistical analysis of taxonomic and functional profiles Parks, Donovan H.; Tyson, Gene W.; Hugenholtz, Philip Bioinformatics, Vol. 30, Issue 21 https://doi.org/10.1093/bioinformatics/btu494	journal	July 2014
Antibiotics and antibiotic resistance genes in global lakes: A review and meta-analysis Yang, Yuyi; Song, Wenjuan; Lin, Hui Environment International, Vol. 116 https://doi.org/10.1016/j.envint.2018.04.011	journal	July 2018
New Roads Leading to Old Destinations: Efflux Pumps as Targets to Reverse Multidrug Resistance in Bacteria Spengler, Gabriella; Kincses, Annamária; Gajdács, Márió Molecules, Vol. 22, Issue 3 https://doi.org/10.3390/molecules22030468	journal	March 2017
Dissemination of antibiotic resistance genes from antibiotic producers to pathogens Jiang, Xinglin; Ellabaan, Mostafa M. Hashim; Charusanti, Pep Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15784	journal	June 2017
Supercarriers of antibiotic resistome in a world’s large river Wang, Jiawen; Pan, Rui; Dong, Peiyan Microbiome, Vol. 10, Issue 1 https://doi.org/10.1186/s40168-022-01294-z	journal	July 2022
Antibiotic resistance in the environment Larsson, D. G. Joakim; Flach, Carl-Fredrik Nature Reviews Microbiology, Vol. 20, Issue 5 https://doi.org/10.1038/s41579-021-00649-x	journal	November 2021
Genomics and metatranscriptomics of biogeochemical cycling and degradation of lignin-derived aromatic compounds in thermal swamp sediment Levy-Booth, David J.; Hashimi, Ameena; Roccor, Raphael The ISME Journal, Vol. 15, Issue 3 https://doi.org/10.1038/s41396-020-00820-x	journal	November 2020
Antibiotic pollution in surface fresh waters: Occurrence and effects Danner, Marie-Claire; Robertson, Anne; Behrends, Volker Science of The Total Environment, Vol. 664 https://doi.org/10.1016/j.scitotenv.2019.01.406	journal	May 2019
Polycyclic aromatic hydrocarbons (PAHs) enriching antibiotic resistance genes (ARGs) in the soils Chen, Baowei; He, Rong; Yuan, Ke Environmental Pollution, Vol. 220 https://doi.org/10.1016/j.envpol.2016.11.047	journal	January 2017
Environmental media exert a bottleneck in driving the dynamics of antibiotic resistance genes in modern aquatic environment Chen, Yihan; Li, Peng; Huang, Yuansheng Water Research, Vol. 162 https://doi.org/10.1016/j.watres.2019.06.047	journal	October 2019
Multicenter assessment of microbial community profiling using 16S rRNA gene sequencing and shotgun metagenomic sequencing Han, Dongsheng; Gao, Peng; Li, Rui Journal of Advanced Research, Vol. 26 https://doi.org/10.1016/j.jare.2020.07.010	journal	November 2020
Deciphering of microbial community and antibiotic resistance genes in activated sludge reactors under high selective pressure of different antibiotics Zhao, Renxin; Feng, Jie; Liu, Jie Water Research, Vol. 151 https://doi.org/10.1016/j.watres.2018.12.034	journal	March 2019
Drug Resistance and Gene Transfer Mechanisms in Respiratory/Oral Bacteria Jiang, S.; Zeng, J.; Zhou, X. Journal of Dental Research, Vol. 97, Issue 10 https://doi.org/10.1177/0022034518782659	journal	June 2018
ARGs-OAP v2.0 with an expanded SARG database and Hidden Markov Models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes Yin, Xiaole; Jiang, Xiao-Tao; Chai, Benli Bioinformatics, Vol. 34, Issue 13 https://doi.org/10.1093/bioinformatics/bty053	journal	February 2018
High-throughput profiling and analysis of antibiotic resistance genes in East Tiaoxi River, China Zheng, Ji; Gao, Ruixia; Wei, Yuanyuan Environmental Pollution, Vol. 230 https://doi.org/10.1016/j.envpol.2017.07.025	journal	November 2017
NCycDB: a curated integrative database for fast and accurate metagenomic profiling of nitrogen cycling genes Tu, Qichao; Lin, Lu; Cheng, Lei Bioinformatics, Vol. 35, Issue 6 https://doi.org/10.1093/bioinformatics/bty741	journal	August 2018
Periodontal pathogens and tetracycline resistance genes in subgingival biofilm of periodontally healthy and diseased Dominican adults Collins, James R.; Arredondo, Alexandre; Roa, Alma Clinical Oral Investigations, Vol. 20, Issue 2 https://doi.org/10.1007/s00784-015-1516-2	journal	June 2015
The antibiotic resistome of free-living and particle-attached bacteria under a reservoir cyanobacterial bloom Guo, Yunyan; Liu, Min; Liu, Lemian Environment International, Vol. 117 https://doi.org/10.1016/j.envint.2018.04.045	journal	August 2018
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
New insights from uncultivated genomes of the global human gut microbiome Nayfach, Stephen; Shi, Zhou Jason; Seshadri, Rekha Nature, Vol. 568, Issue 7753 https://doi.org/10.1038/s41586-019-1058-x	journal	March 2019
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Predominant role of msr(D) over mef(A) in macrolide resistance in Streptococcus pyogenes Zhang, Yan; Tatsuno, Ichiro; Okada, Ryo Microbiology, Vol. 162, Issue 1 https://doi.org/10.1099/mic.0.000206	journal	January 2016
Bacterial Responses and Genome Instability Induced by Subinhibitory Concentrations of Antibiotics Laureti, Luisa; Matic, Ivan; Gutierrez, Arnaud Antibiotics, Vol. 2, Issue 1 https://doi.org/10.3390/antibiotics2010100	journal	March 2013
Small-scale wastewater treatment plants as a source of the dissemination of antibiotic resistance genes in the aquatic environment Osińska, Adriana; Korzeniewska, Ewa; Harnisz, Monika Journal of Hazardous Materials, Vol. 381 https://doi.org/10.1016/j.jhazmat.2019.121221	journal	January 2020
The importance of efflux pumps in bacterial antibiotic resistance Webber, M. A. Journal of Antimicrobial Chemotherapy, Vol. 51, Issue 1 https://doi.org/10.1093/jac/dkg050	journal	December 2002
Distribution and ecological risk of antibiotics in a typical effluent–receiving river (Wangyang River) in north China Jiang, Yonghai; Li, Mingxiao; Guo, Changsheng Chemosphere, Vol. 112 https://doi.org/10.1016/j.chemosphere.2014.04.075	journal	October 2014
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Occurrence and persistence of antibiotic resistance genes in river biofilms after wastewater inputs in small rivers Proia, Lorenzo; von Schiller, Daniel; Sànchez-Melsió, Alexandre Environmental Pollution, Vol. 210 https://doi.org/10.1016/j.envpol.2015.11.035	journal	March 2016
Profiling of emerging pathogens, antibiotic resistance genes and mobile genetic elements in different biological wastewater treatment plants Conco, Thobela; Kumari, Sheena; Awolusi, Oluyemi Olatunji Journal of Environmental Chemical Engineering, Vol. 10, Issue 3 https://doi.org/10.1016/j.jece.2022.107596	journal	June 2022
Breastmilk influences development and composition of the oral microbiome Butler, Catherine A.; Adams, Geoffrey G.; Blum, Jordan Journal of Oral Microbiology, Vol. 14, Issue 1 https://doi.org/10.1080/20002297.2022.2096287	journal	July 2022
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis Uritskiy, Gherman V.; DiRuggiero, Jocelyne; Taylor, James Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0541-1	journal	September 2018
Efflux-Mediated Drug Resistance in Bacteria: An Update Li, Xian-Zhi; Nikaido, Hiroshi Drugs, Vol. 69, Issue 12 https://doi.org/10.2165/11317030-000000000-00000	journal	January 2009
Climate Change Will Affect the Asian Water Towers Immerzeel, W. W.; van Beek, L. P. H.; Bierkens, M. F. P. Science, Vol. 328, Issue 5984 https://doi.org/10.1126/science.1183188	journal	June 2010
A review of computational tools for generating metagenome-assembled genomes from metagenomic sequencing data Yang, Chao; Chowdhury, Debajyoti; Zhang, Zhenmiao Computational and Structural Biotechnology Journal, Vol. 19 https://doi.org/10.1016/j.csbj.2021.11.028	journal	January 2021
Profiling the antibiotic resistome in soils between pristine and human-affected sites on the Tibetan Plateau Wang, Hang; Su, Xiaoxuan; Su, Jianqiang Journal of Environmental Sciences, Vol. 111 https://doi.org/10.1016/j.jes.2021.04.019	journal	January 2022
The molecular basis, genetic control and pleiotropic effects of local gene co-expression Ribeiro, Diogo M.; Rubinacci, Simone; Ramisch, Anna Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-25129-x	journal	August 2021
Bacterial Multidrug Efflux Pumps: Much More Than Antibiotic Resistance Determinants Blanco, Paula; Hernando-Amado, Sara; Reales-Calderon, Jose Microorganisms, Vol. 4, Issue 1 https://doi.org/10.3390/microorganisms4010014	journal	February 2016
Characteristics and Driving Factors of the Aerobic Denitrifying Microbial Community in Baiyangdian Lake, Xiong’an New Area Zhou, Shilei; Sun, Yue; Li, Zaixing Microorganisms, Vol. 8, Issue 5 https://doi.org/10.3390/microorganisms8050714	journal	May 2020
Metagenomic biomarker discovery and explanation Segata, Nicola; Izard, Jacques; Waldron, Levi Genome Biology, Vol. 12, Issue 6 https://doi.org/10.1186/gb-2011-12-6-r60	journal	January 2011
Mechanisms of bacterial persistence during stress and antibiotic exposure Harms, Alexander; Maisonneuve, Etienne; Gerdes, Kenn Science, Vol. 354, Issue 6318 https://doi.org/10.1126/science.aaf4268	journal	December 2016
Bacterial community and climate change implication affected the diversity and abundance of antibiotic resistance genes in wetlands on the Qinghai-Tibetan Plateau Yang, Yuyi; Liu, Guihua; Ye, Chen Journal of Hazardous Materials, Vol. 361 https://doi.org/10.1016/j.jhazmat.2018.09.002	journal	January 2019
The effect of ultralow-dose antibiotics exposure on soil nitrate and N2O flux DeVries, Stephanie L.; Loving, Madeline; Li, Xiqing Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16818	journal	November 2015
Fast Genome-Wide Functional Annotation through Orthology Assignment by eggNOG-Mapper Huerta-Cepas, Jaime; Forslund, Kristoffer; Coelho, Luis Pedro Molecular Biology and Evolution, Vol. 34, Issue 8 https://doi.org/10.1093/molbev/msx148	journal	April 2017
Pathogenic and Indigenous Denitrifying Bacteria are Transcriptionally Active and Key Multi-Antibiotic-Resistant Players in Wastewater Treatment Plants Yuan, Ling; Wang, Yubo; Zhang, Lu Environmental Science & Technology, Vol. 55, Issue 15 https://doi.org/10.1021/acs.est.1c02483	journal	July 2021
Major New Microbial Groups Expand Diversity and Alter our Understanding of the Tree of Life Castelle, Cindy J.; Banfield, Jillian F. Cell, Vol. 172, Issue 6 https://doi.org/10.1016/j.cell.2018.02.016	journal	March 2018
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
High-throughput profiling of seasonal variations of antibiotic resistance gene transport in a peri-urban river Zheng, Ji; Zhou, Zhenchao; Wei, Yuanyuan Environment International, Vol. 114 https://doi.org/10.1016/j.envint.2018.02.039	journal	May 2018
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
Antibiotic resistance genes in treated wastewater and in the receiving water bodies: A pan-European survey of urban settings Cacace, Damiano; Fatta-Kassinos, Despo; Manaia, Celia M. Water Research, Vol. 162 https://doi.org/10.1016/j.watres.2019.06.039	journal	October 2019
Towards standards for human fecal sample processing in metagenomic studies Costea, Paul I.; Zeller, Georg; Sunagawa, Shinichi Nature Biotechnology, Vol. 35, Issue 11 https://doi.org/10.1038/nbt.3960	journal	October 2017
Fate of antibiotic resistance genes and their associations with bacterial community in livestock breeding wastewater and its receiving river water Jia, Shuyu; Zhang, Xu-Xiang; Miao, Yu Water Research, Vol. 124 https://doi.org/10.1016/j.watres.2017.07.061	journal	November 2017
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes Ju, Feng; Beck, Karin; Yin, Xiaole The ISME Journal, Vol. 13, Issue 2 https://doi.org/10.1038/s41396-018-0277-8	journal	September 2018
Ab initio gene identification in metagenomic sequences Zhu, Wenhan; Lomsadze, Alexandre; Borodovsky, Mark Nucleic Acids Research, Vol. 38, Issue 12 https://doi.org/10.1093/nar/gkq275	journal	April 2010
Antibiotic resistance genes on the Qinghai-Tibet Plateau above an elevation of 5,000 m Wang, Xiaomin; Han, Chang; Lan, Bangrui Environmental Science and Pollution Research, Vol. 29, Issue 3 https://doi.org/10.1007/s11356-021-16007-6	journal	August 2021
Bayesian community-wide culture-independent microbial source tracking Knights, Dan; Kuczynski, Justin; Charlson, Emily S. Nature Methods, Vol. 8, Issue 9 https://doi.org/10.1038/nmeth.1650	journal	July 2011
How effective are strategies to control the dissemination of antibiotic resistance in the environment? A systematic review Goulas, Anaïs; Belhadi, Drifa; Descamps, Alexandre Environmental Evidence, Vol. 9, Issue 1 https://doi.org/10.1186/s13750-020-0187-x	journal	February 2020
How quantitative is metabarcoding: A meta‐analytical approach Lamb, Philip D.; Hunter, Ewan; Pinnegar, John K. Molecular Ecology, Vol. 28, Issue 2 https://doi.org/10.1111/mec.14920	journal	December 2018
Antibiotic resistance genes in an urban river as impacted by bacterial community and physicochemical parameters Zhou, Zhen-Chao; Zheng, Ji; Wei, Yuan-Yuan Environmental Science and Pollution Research, Vol. 24, Issue 30 https://doi.org/10.1007/s11356-017-0032-0	journal	September 2017
Characterization and Demonstration of Mock Communities as Control Reagents for Accurate Human Microbiome Community Measurements Tourlousse, Dieter M.; Narita, Koji; Miura, Takamasa Microbiology Spectrum, Vol. 10, Issue 2 https://doi.org/10.1128/spectrum.01915-21	journal	April 2022

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59 BASIC BIOLOGICAL SCIENCES
Urban river
Qinghai-tibet plateau
Metagenome-assembled genomes
Nitrate reduction
Antibiotic resistance
Sulphonamides

Title: Insight into co-hosts of nitrate reduction genes and antibiotic resistance genes in an urban river of the qinghai-tibet plateau

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