{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T03:09:34Z","timestamp":1792120174569,"version":"4.4.0"},"reference-count":46,"publisher":"American Chemical Society (ACS)","issue":"4","license":[{"start":{"date-parts":[[2015,2,23]],"date-time":"2015-02-23T00:00:00Z","timestamp":1424649600000},"content-version":"vor","delay-in-days":34,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_ccby_termsofuse.html"}],"funder":[{"DOI":"10.13039\/100004325","name":"AstraZeneca","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/100004325","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/F008473\/1"],"award-info":[{"award-number":["EP\/F008473\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/I002154\/1"],"award-info":[{"award-number":["EP\/I002154\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/K004689\/1"],"award-info":[{"award-number":["EP\/K004689\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2015,2,17]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Effective domestic wastewater treatment is among our primary defenses against the dissemination of infectious waterborne disease. However, reducing the amount of energy used in treatment processes has become essential for the future. One low-energy treatment option is anaerobic\u2013aerobic sequence (AAS) bioreactors, which use an anaerobic pretreatment step (e.g., anaerobic hybrid reactors) to reduce carbon levels, followed by some form of aerobic treatment. Although AAS is common in warm climates, it is not known how its compares to other treatment options relative to disease transmission, including its influence on antibiotic resistance (AR) in treated effluents. Here, we used metagenomic approaches to contrast the fate of antibiotic-resistant genes (ARG) in anaerobic, aerobic, and AAS bioreactors treating domestic wastewater. Five reactor configurations were monitored for 6 months, and treatment performance, energy use, and ARG abundance and diversity were compared in influents and effluents. AAS and aerobic reactors were superior to anaerobic units in reducing ARG-like sequence abundances, with effluent ARG levels of 29, 34, and 74 ppm (198 ppm influent), respectively. AAS and aerobic systems especially reduced aminoglycoside, tetracycline, and \u03b2-lactam ARG levels relative to anaerobic units, although 63 persistent ARG subtypes were detected in effluents from all systems (of 234 assessed). Sulfonamide and chloramphenicol ARG levels were largely unaffected by treatment, whereas a broad shift from target-specific ARGs to ARGs associated with multi-drug resistance was seen across influents and effluents. AAS reactors show promise for future applications because they can reduce more ARGs for less energy (32% less energy here), but all three treatment options have limitations and need further study.<\/jats:p>","DOI":"10.1021\/es505521w","type":"journal-article","created":{"date-parts":[[2015,1,20]],"date-time":"2015-01-20T18:11:55Z","timestamp":1421777515000},"page":"2577-2584","source":"Crossref","is-referenced-by-count":187,"title":["Metagenomics\nShows That Low-Energy Anaerobic\u2212Aerobic\nTreatment Reactors Reduce Antibiotic Resistance Gene Levels from Domestic\nWastewater"],"prefix":"10.1021","volume":"49","author":[{"given":"Beate","family":"Christgen","sequence":"first","affiliation":[{"name":"Newcastle University , , ,","place":["Newcastle upon Tyne, United Kingdom, NE1 7RU"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Yang","sequence":"additional","affiliation":[{"name":"University of Hong Kong , , ,","place":["Pok Fu Lam, Hong Kong, People\u2019s Republic of China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. Z.","family":"Ahammad","sequence":"additional","affiliation":[{"name":"Newcastle University , , ,","place":["Newcastle upon Tyne, United Kingdom, NE1 7RU"]},{"name":"Indian Institute of Technology Delhi , , Hauz Khas, , ,","place":["New Delhi, Delhi, India, 110016"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing","family":"Li","sequence":"additional","affiliation":[{"name":"University of Hong Kong , , ,","place":["Pok Fu Lam, Hong Kong, People\u2019s Republic of China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D. Catalina","family":"Rodriquez","sequence":"additional","affiliation":[{"name":"Newcastle University , , ,","place":["Newcastle upon Tyne, United Kingdom, NE1 7RU"]},{"name":"University of Antioquia , , , ,","place":["Medellin, Antioquia, Colombia"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tong","family":"Zhang","sequence":"additional","affiliation":[{"name":"University of Hong Kong , , ,","place":["Pok Fu Lam, Hong Kong, People\u2019s Republic of China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David W.","family":"Graham","sequence":"additional","affiliation":[{"name":"Newcastle University , , ,","place":["Newcastle upon Tyne, United Kingdom, NE1 7RU"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2015,1,20]]},"reference":[{"issue":"2","key":"2026090113413741100_cit1","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1002\/abio.370190205","article-title":"Process engineering\nin biological aerobic waste-water\ntreatment","volume":"19","author":"Gavrilescu","year":"1999","journal-title":"Acta Biotechnol."},{"key":"2026090113413741100_cit2","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.biortech.2013.03.185","article-title":"Anaerobic\u2013aerobic\nsequencing bioreactors improve energy efficiency for treatment of\npersonal care product industry wastes","volume":"139","author":"Ahammad","year":"2013","journal-title":"Bioresour.\nTechnol."},{"issue":"1\u20132","key":"2026090113413741100_cit3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.cej.2009.06.041","article-title":"A review on anaerobic\u2013aerobic\ntreatment of industrial and municipal wastewater","volume":"155","author":"Chan","year":"2009","journal-title":"Chem. Eng. J."},{"issue":"10","key":"2026090113413741100_cit4","doi-asserted-by":"crossref","first-page":"3299","DOI":"10.1016\/j.biortech.2009.12.039","article-title":"Sequential\nanaerobic\u2013aerobic treatment for domestic wastewater\u2500A\nreview","volume":"101","author":"Kassab","year":"2010","journal-title":"Bioresour. Technol."},{"issue":"10","key":"2026090113413741100_cit5","doi-asserted-by":"crossref","first-page":"181","DOI":"10.2166\/wst.2002.0324","article-title":"Anaerobic\ntreatment of domestic sewage: Established technologies and perspectives","volume":"45","author":"Foresti","year":"2002","journal-title":"Water Sci. Technol."},{"issue":"17","key":"2026090113413741100_cit6","doi-asserted-by":"crossref","first-page":"2225","DOI":"10.1016\/j.biortech.2005.05.015","article-title":"Anaerobic and complementary treatment of domestic sewage\nin regions with hot climates\u2500A review","volume":"97","author":"Aiyuk","year":"2006","journal-title":"Bioresour. Technol."},{"issue":"9","key":"2026090113413741100_cit7","doi-asserted-by":"crossref","first-page":"67","DOI":"10.2166\/wst.1993.0179","article-title":"Anaerobic treatment of domestic sewage\nand wastewater","volume":"27","author":"Lettinga","year":"1993","journal-title":"Water Sci. Technol."},{"issue":"2","key":"2026090113413741100_cit8","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/j.watres.2010.08.033","article-title":"Release of\nantibiotic resistant bacteria\nand genes in the effluent and biosolids of five wastewater utilities\nin Michigan","volume":"45","author":"Munir","year":"2011","journal-title":"Water Res."},{"issue":"2","key":"2026090113413741100_cit9","first-page":"324","article-title":"Antibiotic resistance,\nplasmid-mediated quinolone resistance (PMQR)\ngenes and ampC gene in two typical municipal wastewater treatment\nplants","volume":"16","author":"Su","year":"2014","journal-title":"Environ. Sci.: Processes Impacts"},{"issue":"1","key":"2026090113413741100_cit10","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1021\/ez400152e","article-title":"Proliferation of multidrug-resistant\nNew Delhi metallo-\u03b2-lactamase\ngenes in municipal wastewater treatment plants in northern China","volume":"1","author":"Luo","year":"2013","journal-title":"Environ. Sci. Technol. Lett."},{"issue":"2","key":"2026090113413741100_cit11","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.chemosphere.2013.03.021","article-title":"Advanced treatment of urban wastewater\nby UV radiation: Effect on antibiotics and antibiotic-resistant E. coli strains","volume":"92","author":"Rizzo","year":"2013","journal-title":"Chemosphere"},{"issue":"8","key":"2026090113413741100_cit12","doi-asserted-by":"crossref","first-page":"1685","DOI":"10.1016\/S0043-1354(02)00569-9","article-title":"Antibiotic resistance\nof E. coli in sewage and sludge","volume":"37","author":"Reinthaler","year":"2003","journal-title":"Water Res."},{"issue":"5","key":"2026090113413741100_cit13","doi-asserted-by":"crossref","first-page":"533","DOI":"10.2225\/vol9-issue5-fulltext-7","article-title":"Frequency\nof transferable multiple antibiotic resistance amongst coliform bacteria\nisolated from a treated sewage effluent in Antofagasta, Chile","volume":"9","author":"Silva","year":"2006","journal-title":"Electron. J. Biotechnol."},{"key":"2026090113413741100_cit14","first-page":"466","article-title":"Emerging organic\ncontaminants and human health","volume-title":"The Handbook\nof Environmental Chemistry","author":"Barcelo","year":"2010"},{"issue":"22","key":"2026090113413741100_cit15","doi-asserted-by":"crossref","first-page":"9543","DOI":"10.1021\/es202775r","article-title":"Tertiary-treated\nmunicipal wastewater is a significant\npoint source of antibiotic resistance genes into Duluth-Superior Harbor","volume":"45","author":"LaPara","year":"2011","journal-title":"Environ. Sci. Technol."},{"key":"2026090113413741100_cit16","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/S0140-6736(11)60401-7","article-title":"Society\u2019s failure to protect\na precious resource: Antibiotics","volume":"378","author":"Carlet","year":"2011","journal-title":"Lancet"},{"key":"2026090113413741100_cit17","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0960-8524(98)00046-7","article-title":"A review: The anaerobic treatment\nof sewage in UASB\nand EGSB reactors","volume":"65","author":"Seghezzoa","year":"1998","journal-title":"Bioresour. Technol."},{"key":"2026090113413741100_cit18","volume-title":"Standard\nMethods for the Examination of Water & Wastewater","author":"American Public Health Association (APHA), American Water Works Association (AWWA), and Water Environment Federation (WEF).","year":"2005","edition":"21"},{"issue":"17","key":"2026090113413741100_cit19","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped\nBLAST and PSI-BLAST: A new\ngeneration of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"issue":"18","key":"2026090113413741100_cit20","doi-asserted-by":"crossref","first-page":"10197","DOI":"10.1021\/es4017365","article-title":"Exploring variation of antibiotic\nresistance genes in activated sludge over a four-year period through\na metagenomic approach","volume":"47","author":"Yang","year":"2013","journal-title":"Environ. Sci. Technol."},{"issue":"2","key":"2026090113413741100_cit21","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0017038","article-title":"Pyrosequencing\nof antibiotic-contaminated river sediments reveals high levels of\nresistance and gene transfer elements","volume":"6","author":"Kristiansson","year":"2011","journal-title":"PLoS\nOne"},{"issue":"10","key":"2026090113413741100_cit22","article-title":"Plasmid metagenome reveals high levels\nof antibiotic resistance genes and mobile genetic elements in activated\nsludge","volume":"6","author":"Zhang","year":"2011","journal-title":"PLoS One"},{"issue":"9","key":"2026090113413741100_cit23","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1101\/gr.092759.109","article-title":"Circos: An information\naesthetic for comparative genomics","volume":"19","author":"Krzywinski","year":"2009","journal-title":"Genome Res."},{"key":"2026090113413741100_cit24","doi-asserted-by":"crossref","first-page":"17","DOI":"10.3389\/fmicb.2013.00017","article-title":"Aerobic\ndigestion reduces the quantity\nof antibiotic resistance genes in residual municipal wastewater solids","volume":"4","author":"Burch","year":"2013","journal-title":"Front. Microbiol."},{"issue":"3","key":"2026090113413741100_cit25","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1007\/s00253-010-2583-6","article-title":"Factors influencing\nantibiotic resistance burden in\nmunicipal wastewater treatment plants","volume":"87","author":"Novo","year":"2010","journal-title":"Appl.\nMicrobiol. Biotechnol."},{"issue":"1\u20134","key":"2026090113413741100_cit26","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/s11270-009-0171-0","article-title":"Ciprofloxacin\nresistance\nin domestic wastewater treatment plants","volume":"208","author":"Manaia","year":"2010","journal-title":"Water,\nAir, Soil Pollut."},{"issue":"3","key":"2026090113413741100_cit27","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1111\/j.1574-6941.2003.tb01073.x","article-title":"Detection\nof antibiotic-resistant\nbacteria and their resistance genes in wastewater, surface water,\nand drinking water biofilms","volume":"43","author":"Schwartz","year":"2003","journal-title":"FEMS Microbiol.\nEcol."},{"key":"2026090113413741100_cit28","doi-asserted-by":"crossref","first-page":"106","DOI":"10.3389\/fmicb.2012.00106","article-title":"Increased\nlevels of multiresistant bacteria and resistance genes after wastewater\ntreatment and their dissemination into Lake Geneva, Switzerland","volume":"3","author":"Czekalski","year":"2012","journal-title":"Front. Microbiol."},{"key":"2026090113413741100_cit29","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1038\/ismej.2014.8","article-title":"Wastewater\nas a point source of antibiotic-resistance genes in the sediment of\na freshwater lake","volume":"8","author":"Czekalski","year":"2014","journal-title":"ISME J."},{"key":"2026090113413741100_cit30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ecoenv.2013.01.016","article-title":"Detection\nand fate of antibiotic\nresistant bacteria in wastewater treatment plants: A review","volume":"91","author":"Bouki","year":"2013","journal-title":"Ecotoxicol. Environ. Saf."},{"issue":"3","key":"2026090113413741100_cit31","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.copbio.2008.05.006","article-title":"Antibiotics and antibiotic resistance\nin water environments","volume":"19","author":"Baquero","year":"2008","journal-title":"Curr. Opin. Biotechnol."},{"key":"2026090113413741100_cit32","doi-asserted-by":"crossref","first-page":"2151","DOI":"10.1038\/ncomms3151","article-title":"Metagenome-wide analysis\nof antibiotic resistance genes in a large\ncohort of human gut microbiota","volume":"4","author":"Hu","year":"2013","journal-title":"Nat. Commun."},{"issue":"6","key":"2026090113413741100_cit33","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0021644","article-title":"The gut as reservoir of antibiotic\nresistance: Microbial diversity of tetracycline resistance in mother\nand infant","volume":"6","author":"de Vries","year":"2011","journal-title":"PLoS One"},{"issue":"3","key":"2026090113413741100_cit34","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1089\/mdr.2009.0916","article-title":"Distribution\nof tetracycline and erythromycin resistance\ngenes among human oral and fecal metagenomic DNA","volume":"15","author":"Seville","year":"2009","journal-title":"Microb. Drug Resist."},{"key":"2026090113413741100_cit35","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.watres.2014.05.019","article-title":"Fate of antibiotic\nresistance genes in sewage treatment plant revealed by metagenomic\napproach","volume":"62","author":"Yang","year":"2014","journal-title":"Water Res."},{"issue":"1","key":"2026090113413741100_cit36","doi-asserted-by":"crossref","first-page":"73","DOI":"10.2217\/fmb.11.135","article-title":"Insights into antibiotic resistance\nthrough metagenomic\napproaches","volume":"7","author":"Schmieder","year":"2012","journal-title":"Future Microbiol."},{"issue":"6797","key":"2026090113413741100_cit37","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1038\/35021219","article-title":"Molecular\nmechanisms that confer antibacterial drug resistance","volume":"406","author":"Walsh","year":"2000","journal-title":"Nature"},{"issue":"4","key":"2026090113413741100_cit38","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1128\/CMR.5.4.387","article-title":"Bacterial-resistance to tetracycline\u2500Mechanisms,\ntransfer, and clinical significance","volume":"5","author":"Speer","year":"1992","journal-title":"Clin. Microbiol.\nRev."},{"issue":"8","key":"2026090113413741100_cit39","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1038\/nrmicro1464","article-title":"Multidrug-resistance\nefflux pumps\u2500Not just for resistance","volume":"4","author":"Piddock","year":"2006","journal-title":"Nat. Rev. Microbiol."},{"issue":"3","key":"2026090113413741100_cit40","doi-asserted-by":"crossref","first-page":"137","DOI":"10.3390\/medicina47030019","article-title":"Antibiotic\nresistance mechanisms of clinically important bacteria","volume":"47","author":"Giedraitiene","year":"2011","journal-title":"Medicina"},{"issue":"1","key":"2026090113413741100_cit41","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1093\/jac\/dki171","article-title":"Efflux-mediated\nantimicrobial resistance","volume":"56","author":"Poole","year":"2005","journal-title":"J. Antimicrob. Chemother."},{"issue":"1","key":"2026090113413741100_cit42","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1093\/jac\/dkg050","article-title":"The\nimportance of efflux pumps in bacterial antibiotic\nresistance","volume":"51","author":"Webber","year":"2003","journal-title":"J. Antimicrob. Chemother."},{"issue":"10","key":"2026090113413741100_cit43","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/j.addr.2005.04.002","article-title":"Bacterial\nresistance to antibiotics: Enzymatic degradation and modification","volume":"57","author":"Wright","year":"2005","journal-title":"Adv. Drug Delivery Rev."},{"key":"2026090113413741100_cit44","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1128\/MMBR.00056-13","article-title":"Integrons:\nPast, present, and future","volume":"78","author":"Gillings","year":"2014","journal-title":"Microbiol. Mol. Biol.\nRev."},{"issue":"10","key":"2026090113413741100_cit45","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1016\/j.addr.2005.04.003","article-title":"Bacterial\nresistance to antibiotics: Modified target sites","volume":"57","author":"Lambert","year":"2005","journal-title":"Adv. Drug Delivery Rev."},{"issue":"5157","key":"2026090113413741100_cit46","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1126\/science.8153624","article-title":"Inactivation\nof antibiotics and the dissemination of resistance genes","volume":"264","author":"Davies","year":"1994","journal-title":"Science"}],"container-title":["Environmental Science &amp; Technology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/es505521w","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/esthag\/article-pdf\/49\/4\/2577\/7954121\/es505521w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/esthag\/article-pdf\/49\/4\/2577\/7954121\/es505521w.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T17:41:48Z","timestamp":1788284508000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/esthag\/article\/49\/4\/2577\/778622\/Metagenomics-Shows-That-Low-Energy-Anaerobic"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,1,20]]},"references-count":46,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2015,1,20]]},"published-print":{"date-parts":[[2015,2,17]]}},"URL":"https:\/\/doi.org\/10.1021\/es505521w","relation":{},"ISSN":["0013-936X","1520-5851"],"issn-type":[{"value":"0013-936X","type":"print"},{"value":"1520-5851","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,1,20]]}}}