{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T19:18:44Z","timestamp":1773861524578,"version":"3.50.1"},"reference-count":33,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T00:00:00Z","timestamp":1704672000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T00:00:00Z","timestamp":1704672000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japanese Society of Promotion of Science","doi-asserted-by":"crossref","award":["KAKENHI 20H00633"],"award-info":[{"award-number":["KAKENHI 20H00633"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"crossref"}]},{"name":"The Sumitomo Electric Industries Group Corporate Social Responsibility Foundation","award":["Endowed Chair Program"],"award-info":[{"award-number":["Endowed Chair Program"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Microb Ecol"],"published-print":{"date-parts":[[2024,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    The house fly is known to be a vector of antibiotic-resistant bacteria (ARB) in animal farms. It is also possible that the house fly contributes to the spread of ARB and antibiotic resistance genes (ARGs) among various environments. We hypothesized that ARB and ARGs present in marine fish and fishery food may gain access to humans via the house fly. We show herein that pAQU1, a marine bacterial ARG-bearing plasmid, persists in the house fly intestine for 5\u00a0days after fly ingestion of marine bacteria. In the case of\n                    <jats:italic>Escherichia coli<\/jats:italic>\n                    bearing the same plasmid, the persistence period exceeded 7\u00a0days. This interval is sufficient for transmission to human environments, meaning that the house fly is capable of serving as a vector of marine-derived ARGs. Time course monitoring of the house fly intestinal microflora showed that the initial microflora was occupied abundantly with Enterobacteriaceae. Experimentally ingested bacteria dominated the intestinal environment immediately following ingestion; however, after 72\u00a0h, the intestinal microflora recovered to resemble that observed at baseline, when diverse genera of Enterobacteriaceae were seen. Given that pAQU1 in marine bacteria and\n                    <jats:italic>E<\/jats:italic>\n                    .\n                    <jats:italic>coli<\/jats:italic>\n                    were detected in fly excrement (defined here as any combination of feces and regurgitated material) at 7\u00a0days post-bacterial ingestion, we hypothesize that the house fly may serve as a vector for transmission of ARGs from marine items and fish to humans via contamination with fly excrement.\n                  <\/jats:p>","DOI":"10.1007\/s00248-023-02341-4","type":"journal-article","created":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T14:02:08Z","timestamp":1704722528000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Persistence of Marine Bacterial Plasmid in the House Fly (Musca domestica): Marine-Derived Antimicrobial Resistance Genes Have a Chance of Invading the Human Environment"],"prefix":"10.1007","volume":"87","author":[{"given":"Kanoko","family":"Nawata","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aya","family":"Kadoya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Satoru","family":"Suzuki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,1,8]]},"reference":[{"key":"2341_CR1","doi-asserted-by":"publisher","first-page":"5649","DOI":"10.1073\/pnas.1503141112","volume":"112","author":"TP Van Boeckel","year":"2015","unstructured":"Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112:5649\u20135654. https:\/\/doi.org\/10.1073\/pnas.1503141112","journal-title":"Proc Natl Acad Sci USA"},{"key":"2341_CR2","doi-asserted-by":"publisher","unstructured":"Anderson M, Cecchini M, Mossialos E (Eds.) (2020) Challenges in tackling antimicrobial resistance, p. 244. ISBN 9781108864121, Cambridge University Press, https:\/\/doi.org\/10.1017\/9781108864121.","DOI":"10.1017\/9781108864121"},{"key":"2341_CR3","unstructured":"World Health Organization (2015) Global action plan on antimicrobial resistance. ISBN 978 92 4 150976 3. https:\/\/apps.who.int\/iris\/handle\/10665\/193736"},{"key":"2341_CR4","doi-asserted-by":"publisher","first-page":"158","DOI":"10.3389\/fmicb.2011.00158","volume":"2","author":"RI Aminov","year":"2011","unstructured":"Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158. https:\/\/doi.org\/10.3389\/fmicb.2011.00158","journal-title":"Front Microbiol"},{"key":"2341_CR5","doi-asserted-by":"publisher","first-page":"3562","DOI":"10.1128\/AEM.00600-14","volume":"80","author":"L Zurek","year":"2014","unstructured":"Zurek L, Ghosh A (2014) Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Appl Environ Microbiol 80:3562\u20133567. https:\/\/doi.org\/10.1128\/AEM.00600-14","journal-title":"Appl Environ Microbiol"},{"key":"2341_CR6","doi-asserted-by":"publisher","first-page":"2701","DOI":"10.1016\/j.scitotenv.2008.11.056","volume":"407","author":"JP Graham","year":"2009","unstructured":"Graham JP, Price LB, Evans SL, Graczyk TK, Silbergend EK (2009) Antibiotic resistant enterococci and staphylococci isolated from flies collected near confined poultry feeding operations. Sci Total Environ 407:2701\u20132710. https:\/\/doi.org\/10.1016\/j.scitotenv.2008.11.056","journal-title":"Sci Total Environ"},{"key":"2341_CR7","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1089\/mdr.2012.0251","volume":"19","author":"M Usui","year":"2013","unstructured":"Usui M, Iwasa T, Fikuda A, Sato T, Okubo T, Tamura Y (2013) The role of flies in spreading the extended-spectrum \u03b2-lactamase gene from cattle. Microb Drug Resist 19:415\u2013420. https:\/\/doi.org\/10.1089\/mdr.2012.0251","journal-title":"Microb Drug Resist"},{"key":"2341_CR8","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1089\/mdr.2015.0033","volume":"21","author":"M Usui","year":"2015","unstructured":"Usui M, Shirakawa T, Fukuda A, Tamura Y (2015) The role of flies in disseminating plasmids with antimicrobial-resistance genes between farms. Microb Drug Resist 21:562\u2013569. https:\/\/doi.org\/10.1089\/mdr.2015.0033","journal-title":"Microb Drug Resist"},{"key":"2341_CR9","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.tmaid.2018.02.007","volume":"22","author":"FC Onwugamba","year":"2018","unstructured":"Onwugamba FC, Fitzgerald JR, Rochon K, Guardabassi L, Alabi A, K\u00fchne S, Grobusch MP, Schaumburg F (2018) The role of \u2018filth flies\u2019 in the spread of antimicrobial resistance. Travel Med Inf Dis 22:8\u201317. https:\/\/doi.org\/10.1016\/j.tmaid.2018.02.007","journal-title":"Travel Med Inf Dis"},{"key":"2341_CR10","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1007\/s00248-013-0337-6","volume":"67","author":"CW Doud","year":"2014","unstructured":"Doud CW, Scott HM, Zurek L (2014) Role of house flies in the ecology of Enterococcus faecalis from wastewater treatment facilities. Microb Ecol 67:380\u2013391. https:\/\/doi.org\/10.1007\/s00248-013-0337-6","journal-title":"Microb Ecol"},{"key":"2341_CR11","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1264\/jsme2.22.355","volume":"22","author":"L Nonaka","year":"2007","unstructured":"Nonaka L, Ikeno K, Suzuki S (2007) Distribution of tetracycline resistance gene, tet(M), in Gram-positive and Gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan. Microbes Environ 22:355\u2013364. https:\/\/doi.org\/10.1264\/jsme2.22.355","journal-title":"Microbes Environ"},{"key":"2341_CR12","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1016\/j.scitotenv.2019.03.111","volume":"669","author":"S Suzuki","year":"2019","unstructured":"Suzuki S, Nakanishi S, Tamminen M, Yokokawa T, Sato-Takabe Y, Ohta K, Chou H-Y, Muziasari WI, Virta M (2019) Occurrence of sul and tet(M) genes in bacterial community in Japanese marine aquaculture environment throughout the year: profile comparison with Taiwanese and Finnish aquaculture waters. Sci Total Environ 669:649\u2013656. https:\/\/doi.org\/10.1016\/j.scitotenv.2019.03.111","journal-title":"Sci Total Environ"},{"key":"2341_CR13","doi-asserted-by":"publisher","first-page":"1926337","DOI":"10.1080\/20964129.2021.1926337","volume":"7","author":"E-L Thiang","year":"2021","unstructured":"Thiang E-L, Lee C-W, Takada H, Seki K, Takei A, Suzuki S, Wang A, Bong C-W (2021) Antibiotic residues from aquaculture farms and their ecological risks in Southeast Asia: a case study from Malaysia. Ecosyst Health Sust 7:1926337. https:\/\/doi.org\/10.1080\/20964129.2021.1926337","journal-title":"Ecosyst Health Sust"},{"key":"2341_CR14","doi-asserted-by":"publisher","unstructured":"Cuadrat RRC, Sorokina M, Andrade B, Goris T, Avila AMRD (2020) Global ocean resistome revealed: exploring antibiotic resistance gene abundance and distribution in TARA oceans samples. Gigascience 9:giaa046.\u00a0https:\/\/doi.org\/10.1093\/gigascience\/giaa046","DOI":"10.1093\/gigascience\/giaa046"},{"key":"2341_CR15","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.scitotenv.2018.03.305","volume":"634","author":"S Suzuki","year":"2018","unstructured":"Suzuki S, Makihara N, Kadoya A (2018) Tetracycline resistance gene tet(M) of a marine bacterial strains is not accumulated in bivalves from seawater in clam tank experiment and mussel monitoring. Sci Total Environ 634:181\u2013187. https:\/\/doi.org\/10.1016\/j.scitotenv.2018.03.305","journal-title":"Sci Total Environ"},{"key":"2341_CR16","doi-asserted-by":"publisher","first-page":"21878","DOI":"10.1038\/s41598-020-78849-3","volume":"10","author":"D Schar","year":"2020","unstructured":"Schar D, Klein EY, Laxminarayan R, Gilbert M, Boeckel TPV (2020) Global trends in antimicrobial use in aquaculture. Sci Rep 10:21878. https:\/\/doi.org\/10.1038\/s41598-020-78849-3","journal-title":"Sci Rep"},{"key":"2341_CR17","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1021\/es102725n","volume":"45","author":"M Tamminen","year":"2011","unstructured":"Tamminen M, Karkman A, L\u00f5hmus A, Muziasari WI, Takasu H, Wada S, Suzuki S, Virta M (2011) Tetracycline resistance genes persist at aquaculture farms in the absence of selective pressure. Environ Sci Technol 45:386\u2013391. https:\/\/doi.org\/10.1021\/es102725n","journal-title":"Environ Sci Technol"},{"key":"2341_CR18","doi-asserted-by":"publisher","first-page":"21","DOI":"10.3390\/ijerph14010021","volume":"14","author":"MM Songe","year":"2017","unstructured":"Songe MM, Hang\u2019ombe BM, Knight-Jones TJD, Grace D (2017) Antimicrobial resistant enteropathogenic Escherichia coli and Salmonella spp in houseflies infesting fish in food markets in Zambia. Int J Environ Res Public Health. 14:21","journal-title":"Int J Environ Res Public Health."},{"key":"2341_CR19","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1603\/033.046.0116","volume":"46","author":"J McGaughey","year":"2009","unstructured":"McGaughey J, Nayduch D (2009) Temporal and spatial fate of GFP-expressing motile and nonmotile Aeromonas hydrophila in the house fly digestive tract. J Med Entomol 46:123\u2013130. https:\/\/doi.org\/10.1603\/033.046.0116","journal-title":"J Med Entomol"},{"key":"2341_CR20","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1264\/jsme2.ME11338","volume":"27","author":"L Nonaka","year":"2012","unstructured":"Nonaka L, Maruyama F, Miyamoto M, Miyakoshi M, Kurokawa K, Masuda M (2012) Novel conjugative transferable multiple drug resistance plasmid pAQU1 from Photobacterium damselae subsp. damselae isolated from marine aquaculture environment. Microbes Environ 27:263\u2013272. https:\/\/doi.org\/10.1264\/jsme2.ME11338","journal-title":"Microbes Environ"},{"key":"2341_CR21","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1264\/jsme2.ME19099","volume":"34","author":"Y Kohyama","year":"2019","unstructured":"Kohyama Y, Suzuki S (2019) Conjugative gene transfer between nourished and starved cells of Photobacterium damselae ssp. damselae and Escherichia coli. Microbes Environ 34:388\u2013392. https:\/\/doi.org\/10.1264\/jsme2.ME19099","journal-title":"Microbes Environ"},{"key":"2341_CR22","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1264\/jsme2.ME15122","volume":"30","author":"TLT Bien","year":"2015","unstructured":"Bien TLT, Sato-Takabe Y, Ogo M, Usui M, Suzuki S (2015) Persistence of multi-drug resistance plasmids in sterile water under very low concentrations of tetracycline. Microbes Environ 30:339\u2013343. https:\/\/doi.org\/10.1264\/jsme2.ME15122","journal-title":"Microbes Environ"},{"key":"2341_CR23","doi-asserted-by":"publisher","first-page":"4605","DOI":"10.1128\/AEM.66.11.4605-4614.2000","volume":"66","author":"MT Suzuki","year":"2000","unstructured":"Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5\u2019-nuclease assays. Appl Environ Microbiol 66:4605\u20134614. https:\/\/doi.org\/10.1128\/AEM.66.11.4605-4614.2000","journal-title":"Appl Environ Microbiol"},{"key":"2341_CR24","doi-asserted-by":"publisher","first-page":"1571","DOI":"10.1038\/ismej.2011.41","volume":"5","author":"DPR Herlemann","year":"2011","unstructured":"Herlemann DPR, Labrenz M, J\u00fcrgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571\u20131579. https:\/\/doi.org\/10.1038\/ismej.2011.41","journal-title":"ISME J"},{"key":"2341_CR25","doi-asserted-by":"publisher","first-page":"152","DOI":"10.3389\/fmicb.2014.00152","volume":"5","author":"L Nonaka","year":"2014","unstructured":"Nonaka L, Maruyama F, Onishi Y, Kobayashi T, Ogura Y, Hayashi T, Suzuki S, Masuda M (2014) Various pAQU plasmids possibly contribute to disseminate tetracycline resistance gene tet(M) among marine bacterial community. Front Microbiol 5:152. https:\/\/doi.org\/10.3389\/fmicb.2014.00152","journal-title":"Front Microbiol"},{"key":"2341_CR26","doi-asserted-by":"publisher","first-page":"360","DOI":"10.1016\/j.jgar.2022.04.024","volume":"29","author":"S Suzuki","year":"2022","unstructured":"Suzuki S, Kadoya A, Masuda N, Sugimoto Y, Takada H, Mizukawa K, Takei A, Chou H-Y, Wu J-H (2022) Macrolide resistance genes and mobile genetic elements in waterways from pig farms to the sea in Taiwan. J Glob Antimicrob Resist 29:360\u2013370. https:\/\/doi.org\/10.1016\/j.jgar.2022.04.024","journal-title":"J Glob Antimicrob Resist"},{"key":"2341_CR27","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1007\/s11274-009-0004-8","volume":"25","author":"AF Neela","year":"2009","unstructured":"Neela AF, Nonaka L, Rahman MH, Suzuki S (2009) Transfer of the chromosomally encoded tetracycline resistance gene tet(M) from marine bacteria to Escherichia coli and Enterococcus faecalis. World J Microbiol Biotechnol 25:1095\u20131101. https:\/\/doi.org\/10.1007\/s11274-009-0004-8","journal-title":"World J Microbiol Biotechnol"},{"key":"2341_CR28","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/S1286-4579(01)01371-5","volume":"3","author":"TK Graczyk","year":"2001","unstructured":"Graczyk TK, Knight R, Gilman RH, Cranfield MR (2001) The role of non-biting flies in the epidemiology of human infectious diseases. Microbes Infect 3:231\u2013235. https:\/\/doi.org\/10.1016\/S1286-4579(01)01371-5","journal-title":"Microbes Infect"},{"key":"2341_CR29","doi-asserted-by":"publisher","first-page":"7445","DOI":"10.1021\/es060413l","volume":"40","author":"A Pruden","year":"2006","unstructured":"Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in northern Colorado. Environ Sci Technol 40:7445\u20137450. https:\/\/doi.org\/10.1021\/es060413l","journal-title":"Environ Sci Technol"},{"key":"2341_CR30","doi-asserted-by":"publisher","first-page":"3705","DOI":"10.1016\/j.watres.2004.06.015","volume":"38","author":"M Rysz","year":"2004","unstructured":"Rysz M, Alvarez PJJ (2004) Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Res 38:3705\u20133712. https:\/\/doi.org\/10.1016\/j.watres.2004.06.015","journal-title":"Water Res"},{"key":"2341_CR31","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/j.femsle.2004.06.026","volume":"237","author":"S-R Kim","year":"2004","unstructured":"Kim S-R, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance genes tet(M) and tet(S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237:147\u2013156. https:\/\/doi.org\/10.1016\/j.femsle.2004.06.026","journal-title":"FEMS Microbiol Lett"},{"key":"2341_CR32","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1089\/mdr.2017.0371","volume":"25","author":"A Fukuda","year":"2019","unstructured":"Fukuda A, Usui M, Okamura M, Dong-Liang H, Tamura Y (2019) The role of flies in the maintenance of antimicrobial resistance in farm environments. Microb Drug Resist 25:127\u2013132. https:\/\/doi.org\/10.1089\/mdr.2017.0371","journal-title":"Microb Drug Resist"},{"key":"2341_CR33","doi-asserted-by":"publisher","DOI":"10.1016\/j.envint.2020.105834","volume":"142","author":"C Liu","year":"2020","unstructured":"Liu C, Yao H, Chapman SJ, Su J, Wanf C (2020) Changes in gut bacterial communities and the incidence of antibiotic resistance genes during degradation of antibiotics by black soldier fly larvae. Environ Int 142:105834. https:\/\/doi.org\/10.1016\/j.envint.2020.105834","journal-title":"Environ Int"}],"container-title":["Microbial Ecology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00248-023-02341-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00248-023-02341-4\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00248-023-02341-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,8]],"date-time":"2024-01-08T14:02:14Z","timestamp":1704722534000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00248-023-02341-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,8]]},"references-count":33,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,12]]}},"alternative-id":["2341"],"URL":"https:\/\/doi.org\/10.1007\/s00248-023-02341-4","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-3460436\/v1","asserted-by":"object"}]},"ISSN":["0095-3628","1432-184X"],"issn-type":[{"value":"0095-3628","type":"print"},{"value":"1432-184X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,8]]},"assertion":[{"value":"18 October 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 December 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 January 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"30"}}