Escherichia coli phylogroup distribution and prevalence of extended spectrum ß-lactamase (ESBL) producers in U.S. Mid-Atlantic surface and reclaimed water

Authors: SOLAIMAN, SULTANA - University Of Maryland; HANDY, ERIC - Collaborator; BRINKS, TAYLOR - University Of Maryland; GOOD, KASEY - University Of Maryland; BOLLINGER, CHRIS - University Of Maryland; SAPKOTA, AMY - University Of Maryland; Sharma, Manan; MICALLEF, SHIRLEY - University Of Maryland

Submitted to: Applied and Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/18/2022
Publication Date: 7/12/2022
Citation: Solaiman, S., Handy, E., Brinks, T., Good, K., Bollinger, C., Sapkota, A.R., Sharma, M., Micallef, S.A. 2022. Escherichia coli phylogroup distribution and prevalence of extended spectrum ß-lactamase (ESBL) producers in U.S. Mid-Atlantic surface and reclaimed water. Environmental Microbiology. https://doi.org/10.1128/AEM.00837-22.
DOI: https://doi.org/10.1128/AEM.00837-22

Interpretive Summary: As surface water is increasingly used for agricultural irrigation in the U.S., the microbial water quality of different irrigation water types receives additional attention. The most common indicator or water quality is the quantitative level of Escherichia coli, a bacterial indicator of fecal contamination of water. Phylotyping of E. coli - identifying which broad genetic group (A, B1, B2, or D) individual E. coli isolates belong to, can also provide information about the microbial ecology and diversity of the water source. Examining and evaluating the antibiotic resistance of E. coli isolates collected from water sources can also provide information about the contamination levels of antibiotic resistance bacteria in the environment. In all, 488 E. coli isolates from rivers, ponds and reclaimed (recycled wastewater) were examined. E. coli isolates belonging to phylogroup B1 were the most prevalent, while isolates in phylogroup A were the least prevalent. In general, pond water showed more diversity in their E. coli isolates than those river or reclaimed water. Resistance to extended spectrum beta-lactam antibiotics was observed in 3.9% (n=16) of E. coli isolates. Antibiotic-resistant E. coli isolates were observed more frequently in river water compared to in pond or reclaimed water. Overall, resistance to cefotaxime, ceftriaxone, cefuroxime and ceftazidime, and genetic determinants for extended spectrum ß-lactamase (ESBL)-mediated resistance were found predominantly in B2 and D isolates from rivers and reclaimed water. This research helps farmers assess the hazards in their potential irrigation water sources, and provides them information on which sources are more likely to introduce antibiotic-resistant E. coli to fruits and vegetables irrigated with surface water.

Technical Abstract: Phylogenetic distribution and extended spectrum ß-lactamase (ESBL) activity of Escherichia coli recovered from surface and reclaimed water in the mid-Atlantic U.S. were evaluated. Among 488 unique isolates, phylogroups B1 and A were the most and least prevalent, respectively. Water type, but not season, affected phylogroup distribution. Homogeneity in group distribution was lowest in pond water, where group B1 comprised 50% of isolates. Only 16 (3.3%) isolates exhibited phenotypic resistance to one or more ß-lactam antibiotic. Phylogroup was a factor in antimicrobial resistance, with group A (8.7%) and D (1.6%) exhibiting the highest and lowest rates. Resistance to cefoxitin was the most prevalent. Multi- versus single drug resistance was affected by phylogroup and more likely in groups D and B1 than A. The most detected ß-lactam resistance genes were blaCMY-2 and blaTEM. Season affected phenotypic resistance while water type was a factor for blaCTX-M gene detection. Phenotypic resistance to cefotaxime, ceftriaxone, cefuroxime and ceftazidime, and genetic determinants for ESBL-mediated resistance were found predominantly in B2 and D isolates from rivers and reclaimed water. Overall, however, ESBL producers had low prevalence. Integrating data on ß-lactam resistance among E. coli populations can inform decisions on safety of irrigation water sources and One health.