{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T20:02:57Z","timestamp":1760385777700,"version":"build-2065373602"},"reference-count":54,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,7,10]],"date-time":"2020-07-10T00:00:00Z","timestamp":1594339200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>We assessed the prevalence of antimicrobial resistance and screened for clinically relevant \u03b2-lactamase resistance determinants in Gram-negative bacteria from a large urbanized estuary. In contrast to the broad literature documenting potentially hazardous resistance determinants near wastewater treatment discharge points and other local sources of aquatic pollution, we employed a probabilistic survey design to examine ambient, near-shore sediments. We plated environmental samples from 40 intertidal and shallow subtidal areas around San Francisco Bay (California, USA) on drug-supplemented MacConkey agar, and we tested isolates for antimicrobial resistance and presence of clinically relevant \u03b2-lactamase resistance determinants. Of the 74 isolates identified, the most frequently recovered taxa were Vibrio spp. (40%), Shewanella spp. (36%), Pseudomonas spp. (11%), and Aeromonas spp. (4%). Of the 55 isolates tested for antimicrobial resistance, the Vibrio spp. showed the most notable resistance profiles. Most (96%) were resistant to ampicillin, and two isolates showed multidrug-resistant phenotypes: V. alginolyticus (cefotaxime, ampicillin, gentamicin, cefoxitin) and V. fluvialis (cefotaxime, ampicillin, cefoxitin). Targeted testing for class 1 integrons and presence of \u03b2-lactam-resistance gene variants TEM, SHV, OXA, CTX-M, and Klebsiella pneumonia carbapenemase (KPC) did not reveal any isolates harboring these resistance determinants. Thus, while drug-resistant, Gram-negative bacteria were recovered from ambient sediments, neither clinically relevant strains nor mobile \u03b2-lactam resistance determinants were found. This suggests that Gram-negative bacteria in this well-managed, urbanized estuary are unlikely to constitute a major human exposure hazard at this time.<\/jats:p>","DOI":"10.3390\/antibiotics9070400","type":"journal-article","created":{"date-parts":[[2020,7,10]],"date-time":"2020-07-10T09:25:28Z","timestamp":1594373128000},"page":"400","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Antimicrobial Drug-Resistant Gram-Negative Saprophytic Bacteria Isolated from Ambient, Near-Shore Sediments of an Urbanized Estuary: Absence of \u03b2-Lactamase Drug-Resistance Genes"],"prefix":"10.3390","volume":"9","author":[{"given":"Charles F.","family":"Moritz","sequence":"first","affiliation":[{"name":"School of Public Health, University of California, Berkeley, CA 94720, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9743-0872","authenticated-orcid":false,"given":"Robert E.","family":"Snyder","sequence":"additional","affiliation":[{"name":"School of Public Health, University of California, Berkeley, CA 94720, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lee W.","family":"Riley","sequence":"additional","affiliation":[{"name":"School of Public Health, University of California, Berkeley, CA 94720, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Devin W.","family":"Immke","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences, Southern Illinois University, Edwardsville, IL 62026, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1038-7635","authenticated-orcid":false,"given":"Ben K.","family":"Greenfield","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences, Southern Illinois University, Edwardsville, IL 62026, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,7,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1016\/j.jenvman.2013.06.051","article-title":"Extended-Spectrum Beta-Lactamase (ESBL)-Positive Enterobacteriaceae in Municipal Sewage and Their Emission to the Environment","volume":"128","author":"Korzeniewska","year":"2013","journal-title":"J. Environ. Manage."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1128\/AEM.66.1.125-132.2000","article-title":"Impact of an Urban Effluent on Antibiotic Resistance of Riverine Enterobacteriaceae and Aeromonas Spp","volume":"66","author":"Capdepuy","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1289\/ehp.1104650","article-title":"Selective Pressure of Antibiotic Pollution on Bacteria of Importance to Public Health","volume":"120","author":"Tello","year":"2012","journal-title":"Environ. Health Perspect."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1093\/jac\/dku079","article-title":"Waste Water Effluent Contributes to the Dissemination of CTX-M-15 in the Natural Environment","volume":"69","author":"Amos","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1864","DOI":"10.1001\/jama.2016.4151","article-title":"Prevalence of Inappropriate Antibiotic Prescriptions among Us Ambulatory Care Visits, 2010\u20132011","volume":"315","author":"Hersh","year":"2016","journal-title":"JAMA-J. Am. Med. Assoc."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"16270","DOI":"10.1038\/nmicrobiol.2016.270","article-title":"Continental-Scale Pollution of Estuaries with Antibiotic Resistance Genes","volume":"2","author":"Zhu","year":"2017","journal-title":"Nat. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Laxminarayan, R., Duse, A., Wattal, C., Zaidi, A.K.M., Wertheim, H.F.L., Sumpradit, N., Vlieghe, E., Hara, G.L., Gould, I.M., and Goossens, H. (2013). Antibiotic Resistance-the Need for Global Solutions. Lancet Infect. Dis., 1057\u20131098.","DOI":"10.1016\/S1473-3099(13)70318-9"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Nagvekar, V., Sawant, S., and Amey, S. (2020). Prevalence of Multi Drug Resistant Gram-Negative Bacteria Cases at Admission in Multispecialty Hospital. J. Glob. Antimicrob. Resist.","DOI":"10.1016\/j.jgar.2020.02.030"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Fasciana, T., Gentile, B., Aquilina, M., Ciammaruconi, A., Mascarella, C., Anselmo, A., Fortunato, A., Fillo, S., Petralito, G., and Lista, F. (2019). Co-Existence of Virulence Factors and Antibiotic Resistance in New Klebsiella Pneumoniae Clones Emerging in South of Italy. BMC Infect. Dis., 19.","DOI":"10.1186\/s12879-019-4565-3"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1099\/jmm.0.041970-0","article-title":"Globally Dispersed Mobile Drug-Resistance Genes in Gram-Negative Bacterial Isolates from Patients with Bloodstream Infections in a US Urban General Hospital","volume":"61","author":"Tartof","year":"2012","journal-title":"J. Med. Microbiol."},{"key":"ref_11","unstructured":"Center for Disease Control and Prevention (2013). Antibiotic Resistance Threats in the United States, Center for Disease Control and Prevention."},{"key":"ref_12","first-page":"28564","article-title":"Environmental Dissemination of Antibiotic Resistance Genes and Correlation to Anthropogenic Contamination with Antibiotics","volume":"5","author":"Berglund","year":"2015","journal-title":"Infect. Ecol. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1128\/MMBR.00016-10","article-title":"Origins and Evolution of Antibiotic Resistance","volume":"74","author":"Davies","year":"2010","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1093\/jac\/dkt392","article-title":"Carbapenemase-Producing Enterobacteriaceae and Non-Enterobacteriaceae from Animals and the Environment: An Emerging Public Health Risk of Our Own Making?","volume":"69","author":"Woodford","year":"2014","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.envint.2015.04.005","article-title":"Does Human Activity Impact the Natural Antibiotic Resistance Background? Abundance of Antibiotic Resistance Genes in 21 Swiss Lakes","volume":"81","author":"Czekalski","year":"2015","journal-title":"Environ. Int."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1128\/AEM.02506-10","article-title":"Extended-Spectrum Beta-Lactamase Gene Sequences in Gram-Negative Saprophytes on Retail Organic and Nonorganic Spinach","volume":"77","author":"Raphael","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.scitotenv.2008.08.014","article-title":"Antibacterial Agents and Heavy Metal Resistance in Gram-Negative Bacteria Isolated from Seawater, Shrimp and Sediment in Iskenderun Bay, Turkey","volume":"407","author":"Matyar","year":"2008","journal-title":"Sci. Total Environ."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Griffin, D.W., Banks, K., Gregg, K., Shedler, S., and Walker, B.K. (2020). Antibiotic Resistance in Marine Microbial Communities Proximal to a Florida Sewage Outfall System. Antibiotics.","DOI":"10.3390\/antibiotics9030118"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1089\/mdr.2015.0072","article-title":"Low Prevalence of Carbapenem-Resistant Bacteria in River Water: Resistance Is Mostly Related to Intrinsic Mechanisms","volume":"21","author":"Correia","year":"2015","journal-title":"Microb. Drug Resist."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"a025247","DOI":"10.1101\/cshperspect.a025247","article-title":"\u03b2-Lactams and \u03b2-Lactamase Inhibitors: An Overview","volume":"6","author":"Bush","year":"2016","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e01076-18","DOI":"10.1128\/AAC.01076-18","article-title":"Past and Present Perspectives on \u03b2-Lactamases","volume":"62","author":"Bush","year":"2018","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1128\/AAC.01025-12","article-title":"Clonal Composition and Community Clustering of Drug-Susceptible and -Resistant Escherichia Coli Isolates from Bloodstream Infections","volume":"57","author":"Diep","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"4943","DOI":"10.1128\/AAC.00296-11","article-title":"Carbapenems: Past, Present, and Future","volume":"55","author":"Endimiani","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.molmed.2012.03.003","article-title":"Carbapenem Resistance in Enterobacteriaceae: Here Is the Storm!","volume":"18","author":"Nordmann","year":"2012","journal-title":"Trends Mol. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5376","DOI":"10.1128\/AAC.00716-11","article-title":"Environmental Microbiota Represents a Natural Reservoir for Dissemination of Clinically Relevant Metallo-\u03b2-Lactamases","volume":"55","author":"Scotta","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1016\/j.ijantimicag.2014.10.016","article-title":"Occurrence of Carbapenemase-Producing Bacteria in Coastal Recreational Waters","volume":"45","author":"Montezzi","year":"2015","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"5972","DOI":"10.1128\/AEM.00711-10","article-title":"High Diversity of Extended-Spectrum Beta-Lactamase-Producing Bacteria in an Urban River Sediment Habitat","volume":"76","author":"Lu","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_28","unstructured":"Novick, E., and Senn, D.B. (2014). External Nutrient Loads to San Francisco Bay, San Francisco Estuary Institute."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1039\/C5EW00147A","article-title":"A Quantitative Microbial Risk Assessment of Wastewater Treatment Plant Blending: Case Study in San Francisco Bay","volume":"2","author":"Seto","year":"2015","journal-title":"Environ. Sci. Water Res. Technol."},{"key":"ref_30","first-page":"21","article-title":"The Regional Monitoring Program for Water Quality in San Francisco Bay, California, USA: Science in Support of Managing Water Quality","volume":"4","author":"Trowbridge","year":"2016","journal-title":"Reg. Stud. Mar. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2921","DOI":"10.1016\/j.watres.2008.03.006","article-title":"Fecal Indicator Bacteria and Salmonella in Ponds Managed as Bird Habitat, San Francisco Bay, California, USA","volume":"42","author":"Shellenbarger","year":"2008","journal-title":"Water Res."},{"key":"ref_32","unstructured":"Heal the Bay (2019). 2018\u20132019 Beach Report Card, Heal the Bay."},{"key":"ref_33","unstructured":"San Francisco Estuary Partnership (2015). The State of the Estuary 2015, San Francisco Estuary Partnership."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.diagmicrobio.2013.02.001","article-title":"The Route of Antimicrobial Resistance from the Hospital Effluent to the Environment: Focus on the Occurrence of KPC-Producing Aeromonas Spp. and Enterobacteriaceae in Sewage","volume":"76","author":"Cardoso","year":"2013","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Wang, Z., Zhang, X.-X., Huang, K., Miao, Y., Shi, P., Liu, B., Long, C., and Li, A. (2013). Metagenomic Profiling of Antibiotic Resistance Genes and Mobile Genetic Elements in a Tannery Wastewater Treatment Plant. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0076079"},{"key":"ref_36","unstructured":"Yee, D., Wong, A., Shimabuku, I., and Trowbridge, P. (2017). Characterization of Sediment Contamination in Central Bay Margin Areas, San Francisco Estuary Institute."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Baker-Austin, C., Stockley, L., Rangdale, R., and Martinez-Urtaza, J. (2010). Environmental Occurrence and Clinical Impact of Vibrio Vulnificus and Vibrio Parahaemolyticus: A European Perspective. Environ. Microbiol. Rep., 7\u201318.","DOI":"10.1111\/j.1758-2229.2009.00096.x"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"293","DOI":"10.3109\/1040841X.2012.726209","article-title":"The Genus Shewanella: From the Briny Depths below to Human Pathogen","volume":"40","author":"Janda","year":"2014","journal-title":"Crit. Rev. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1111\/j.1469-0691.2005.01108.x","article-title":"Shewanella Algae and Shewanella Putrefaciens: Clinical and Microbiological Characteristics","volume":"11","author":"Holt","year":"2005","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.ijfoodmicro.2013.07.010","article-title":"Aeromonas Spp. Simultaneously Harbouring BlaCTX-M-15, BlaSHV-12, BlaPER-1 and BlaFOX-2, in Wild-Growing Mediterranean Mussel (Mytilus Galloprovincialis) from Adriatic Sea, Croatia","volume":"166","author":"Cvjetan","year":"2013","journal-title":"Int. J. Food Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/s15010-009-9145-9","article-title":"Population-Based Study of the Epidemiology and the Risk Factors for Pseudomonas Aeruginosa Bloodstream Infection","volume":"38","author":"Parkins","year":"2010","journal-title":"Infection"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1128\/AAC.48.1.348-351.2004","article-title":"Chromosome-Encoded Ambler Class D \u03b2-Lactamase of Shewanella Oneidensis as a Progenitor of Carbapenem-Hydrolyzing Oxacillinase","volume":"48","author":"Poirel","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1093\/jac\/dkp061","article-title":"Identification of BlaIMP-22 in Pseudomonas Spp. in Urban Wastewater and Nosocomial Environments: Biochemical Characterization of a New IMP Metallo-Enzyme Variant and Its Genetic Location","volume":"63","author":"Pellegrini","year":"2009","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"837","DOI":"10.1128\/AAC.45.3.837-844.2001","article-title":"Metallo-\u03b2-Lactamase Producers in Environmental Microbiota: New Molecular Class B Enzyme in Janthinobacterium Lividum","volume":"45","author":"Rossolini","year":"2001","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Shaw, K.S., Rosenberg Goldstein, R.E., He, X., Jacobs, J.M., Crump, B.C., and Sapkota, A.R. (2014). Antimicrobial Susceptibility of Vibrio Vulnificus and Vibrio Parahaemolyticus Recovered from Recreational and Commercial Areas of Chesapeake Bay and Maryland Coastal Bays. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0089616"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1670","DOI":"10.1128\/AAC.48.1.348-351.2004","article-title":"Genetic and Biochemical Characterization of a Chromosome-Encoded Carbapenem-Hydrolyzing Ambler Class D \u03b2-Lactamase from Shewanella Algae","volume":"48","author":"Poirel","year":"2004","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1128\/AAC.00961-09","article-title":"Novel Ambler Class A Carbapenem-Hydrolyzing \u03b2-Lactamase from a Pseudomonas Fluorescens Isolate from the Seine River, Paris, France","volume":"54","author":"Girlich","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2140","DOI":"10.1128\/AAC.49.5.2140-2141.2005","article-title":"First Isolation of BlaVIM-2 in an Environmental Isolate of Pseudomonas Pseudoalcaligenes","volume":"49","author":"Quinteira","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/s12941-015-0100-6","article-title":"Resistance Integrons: Class 1, 2 and 3 Integrons","volume":"14","author":"Deng","year":"2015","journal-title":"Ann. Clin. Microbiol. Antimicrob."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1198\/016214504000000250","article-title":"Spatially Balanced Sampling of Natural Resources","volume":"99","author":"Stevens","year":"2004","journal-title":"J. Am. Stat. Assoc."},{"key":"ref_51","unstructured":"SFEI (2015). Regional Monitoring Program for Water Quality in San Francisco Bay 2015 Bay Margins Sediment Study Cruise Plan, San Francisco Estuary Institute."},{"key":"ref_52","unstructured":"Coastal Contamination & Research (2015). Contaminant Concentrations in Central Bay Margins Sediment Cruise Report, Coastal Contamination & Research."},{"key":"ref_53","unstructured":"CLSI (2015). M100-S25 Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement, Clinical and Laboratory Standards Institute."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1093\/jac\/dkp498","article-title":"Development of a Set of Multiplex PCR Assays for the Detection of Genes Encoding Important \u03b2-Lactamases in Enterobacteriaceae","volume":"65","author":"Dallenne","year":"2010","journal-title":"J. Antimicrob. Chemother."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/7\/400\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:49:51Z","timestamp":1760176191000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/9\/7\/400"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,10]]},"references-count":54,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,7]]}},"alternative-id":["antibiotics9070400"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics9070400","relation":{},"ISSN":["2079-6382"],"issn-type":[{"type":"electronic","value":"2079-6382"}],"subject":[],"published":{"date-parts":[[2020,7,10]]}}}