Architecture of Class 1, 2, and 3 Integrons from Gram Negative Bacteria Recovered among Fruits and Vegetables

Abstract

The spread of antibiotic resistant bacteria throughout the food chain constitutes a public health concern. To understand the contribution of fresh produce in shaping antibiotic resistance bacteria and integron prevalence in the food chain, 333 antibiotic resistance Gram negative isolates were collected from organic and conventionally produced fruits (pears, apples, and strawberries) and vegetables (lettuces, tomatoes, and carrots). Although low levels of resistance have been detected, the bacterial genera identified in the assessed fresh produce are often described not only as environmental, but mostly as commensals and opportunistic pathogens. The genomic characterization of integron-harboring isolates revealed a high number of mobile genetic elements and clinically relevant antibiotic resistance genes, of which we highlight the presence of as mcr-1, qnrA1, bla GES-11, mphA, and oqxAB. The study of class 1 (n = 8), class 2 (n = 3) and class 3 (n = 1) integrons, harbored by species such as Morganella morganii, Escherichia coli, Klebsiella pneumoniae, led to the identification of different integron promoters (PcW, PcH1, PcS, and PcWTNG-10) and cassette arrays (containing drfA, aadA, cmlA, estX, sat, and bla GES). In fact, the diverse integron backbones were associated with transposable elements (e.g., Tn402, Tn7, ISCR1, Tn2 (*), IS26, IS1326, and IS3) that conferred greater mobility. This is also the first appearance of In1258, In1259, and In3-13, which should be monitored to prevent their establishment as successfully dispersed mobile resistance integrons. These results underscore the growing concern about the dissemination of acquired resistance genes by mobile elements in the food chain.

Keywords: agriculture; antibiotic resistance; fresh produce; integrons; mobile genetic elements.

Figure 1

Percentage of bacterial genera recovered from fruits and vegetables.

Figure 2

Schematic representation of regions enclosing class 1 integrons detected among the bacterial population analyzed in the present survey (n = 8/333). (A) E cloacae INSali2 In369; (B) E. cloacae INSali10 In293::ISCR1::qnrA1; (C) E. coli INSali38 In2; (D) E. coli INSali92 In369; (E) M. morgannii INSali207 In1259; (F) E. coli INSali370 In27; (G) K. pneumoniae INSali390 In1258; (H) P. putida INSali382 In0. Green, integron; blue, resistance genes, including gene cassettes; purple, transposons; gray, other genes.

Figure 3

Schematic representation of regions enclosing class 2 integrons detected among the bacterial population analyzed in the present survey (n = 3/333). (A) E. coli INSali25 In2–35; (B) R. planticola INSali127 In2–11; (C) R. planticola INSali133 In2–11. Green, integron; blue, resistance genes, including gene cassettes; purple, transposons; gray, other genes.

Figure 4

Schematic representation of region enclosing In3–13 detected in a K. pneumoniae recovered among the bacterial population analyzed in the present survey (n = 1/333). Green, integron; blue, resistance genes, including gene cassettes; purple, transposons; gray, other genes.