Despite numerous studies on Escherichia coli (E. coli) from sheep, there have been few reports on the characterization of E. coli isolates from various organs of individual sheep until now. The present study conducted molecular typing, antibiotics resistance, biofilm formation, and virulence genes on E. coli isolated from 57 freshly slaughtered apparently healthy sheep carcasses, gallbladders, fecal samples, and mesenteric lymph nodes (MLNs). The results demonstrated that the detection rate of R1 LPS core type in E. coli isolated from fecal samples (70.83%) was higher than that from other organs, but the detection rate of antibiotic resistance genes was lower (P < 0.05). The predominant phylogenetic group of E. coli isolated from the carcasses was group B1 (93.33%), and the detection rate of multidrug-resistance phenotype (80%) and the resistance rate of E. coli was higher than that from other organs (P < 0.05). Interestingly, the intensity of biofilm formation of E. coli isolated from MLNs was higher than that from other organs (P < 0.05). However, except for ibeB, the detection rates of virulence genes did not differ in E.coli isolated from different organs. In conclusion, differences were noted in these parameters of E. coli isolated from different organs of individual sheep. Therefore, the data may contain considerable mistakes concerning the actual situation in the host if we only analyze the data of E. coli isolated from feces or carcasses.

Engineering Laboratory for Tarim Animal Diseases Diagnosis and Control of Xinjiang Production and Construction Corps College of Animal Sciences and Technology Tarim University Alar 86 843300 China

Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin of Xinjiang Production and Construction Corps College of Life Sciences and Technology Tarim University Alar 86 843300 China

See more in PubMed

Abraham S, Gordon DM, Chin J, Brouwers HJM, Njuguna P, Groves MD, Zhang R, Chapman TA (2012) Molecular characterization of commensal Escherichia coli adapted to different compartments of the porcine gastrointestinal tract. Appl Environ Microbiol 78(19):6799–6803. https://doi.org/10.1128/AEM.01688-12 PubMed DOI PMC

Amor K, Heinrichs DE, Frirdich E, Ziebell K, Johnson RP, Whitfield C (2000) Distribution of core oligosaccharide types in lipopolysaccharides from Escherichia coli. Infect Immun 68(3):1116–1124. https://doi.org/10.1128/iai.68.3.1116-1124.2000 PubMed DOI PMC

Appelmelk BJ, An YQ, Hekker TA, Thijs LG, MacLaren DM, de Graaf J (1994) Frequencies of lipopolysaccharide core types in Escherichia coli strains from bacteraemic patients. Microbiology 140(5):1119–1124. https://doi.org/10.1099/13500872-140-5-1119 PubMed DOI

Bass L, Liebert CA, Lee MD, Summers AO, White DG, Thayer SG, Maurer JJ (1999) Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrob Agents Chemother 43(12):2925–2929. https://doi.org/10.1128/AAC.43.12.2925 PubMed DOI PMC

Berg RD, Garlington AW (1979) Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun 23(2):403–411. https://doi.org/10.1128/iai.23.2.403-411.1979 PubMed DOI PMC

Blanco M, Blanco JE, Mora A, Rey J, Alonso JM, Hermoso M, Hermoso J, Alonso MP, Dahbi G, González EA, Bernárdez MI, Blanco J (2003) Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain. J Clin Microbiol 41(4):1351–1356. https://doi.org/10.1128/JCM.41.4.1351-1356.2003 PubMed DOI PMC

Call DR, Bakko MK, Krug MJ, Roberts MC (2003) Identifying antimicrobial resistance genes with DNA microarrays. Antimicrob Agents Chemother 47(10):3290–3295. https://doi.org/10.1128/AAC.47.10.3290-3295.2003 PubMed DOI PMC

Campoccia D, Mirzaei R, Montanaro L, Arciola CR (2019) Hijacking of immune defences by biofilms: a multifront strategy. Biofouling 35(10):1055–1074. https://doi.org/10.1080/08927014.2019.1689964 PubMed DOI

Clermont O, Bonacorsi S, Bingen E (2000) Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66(10):4555–4558. https://doi.org/10.1128/AEM.66.10.4555-4558.2000 PubMed DOI PMC

CLSI (2017) Performance standards for antimicrobial susceptibility testing, 27th ed. CLSI document M100-S27. Clinical Laboratory Standards Institute, Wayne, PA

Connolly JPR, Gabrielsen M, Goldstone RJ, Grinter R, Wang D, Cogdell RJ, Walker D, Smith DGE, Roe AJ (2016) A highly conserved bacterial D-serine uptake system links host metabolism and virulence. PLoS Pathog 12(1):e1005359. https://doi.org/10.1371/journal.ppat.1005359

Currie CG, Poxton IR (1999) The lipopolysaccharide core type of Escherichia coli O157:H7 and other non-O157 verotoxin-producing E. coli. FEMS Immunol Med Microbiol 24(1):57–62. https://doi.org/10.1111/j.1574-695X.1999.tb01265.x

Dissanayake DRA, Wijewardana TG, Gunawardena GA, Poxton IR (2008) Distribution of lipopolysaccharide core types among avian pathogenic Escherichia coli in relation to the major phylogenetic groups. Vet Microbiol 132(3–4):355–363. https://doi.org/10.1016/j.vetmic.2008.05.024 PubMed DOI

Dixit SM, Gordon DM, Wu XY, Chapman T, Kailasapathy K, Chin JJC (2004) Diversity analysis of commensal porcine Escherichia coli-associations between genotypes and habitat in the porcine gastrointestinal tract. Microbiology 150(6):1735–1740. https://doi.org/10.1099/mic.0.26733-0 PubMed DOI

Domingos MO, Melo KCM, Neves IV, Mota CM, Ruiz RC, Melo BS, Lima RC, Horton DSPQ, Borges MM, Franzolin MR (2016) Potential for colonization of O111:H25 atypical enteropathogenic E. coli. J Microbiol 54(11):745–752. https://doi.org/10.1007/s12275-016-6015-x

Doyle D, Peirano G, Lascols C, Lloyd T, Church DL, Pitout JDD (2012) Laboratory detection of Enterobacteriaceae that produce carbapenemases. J Clin Microbiol 50(12):3877–3880. https://doi.org/10.1128/JCM.02117-12 PubMed DOI PMC

Enne VI, Cassar C, Sprigings K, Woodward MJ, Bennett PM (2008) A high prevalence of antimicrobial resistant Escherichia coli isolated from pigs and a low prevalence of antimicrobial resistant E. coli from cattle and sheep in Great Britain at slaughter. FEMS Microbiol Lett 278(2);193–199. https://doi.org/10.1111/j.1574-6968.2007.00991.x

Ewers C, Janssen T, Kiessling S, Philipp HC, Wieler LH (2005) Rapid detection of virulence-associated genes in avian pathogenic Escherichia coli by multiplex polymerase chain reaction. Avian Dis 49(2):269–273. https://doi.org/10.1637/7293-102604R PubMed DOI

Garcia-Tsao G, Lee FY, Barden GE, Cartun R, West AB (1995) Bacterial translocation to mesenteric lymph nodes is increased in cirrhotic rats with ascites. Gastroenterology 108(6):1835–1841. https://doi.org/10.1016/0016-5085(95)90147-7 PubMed DOI

Gibbs RJ, Stewart J, Poxton IR (2004) The distribution of, and antibody response to, the core lipopolysaccharide region of Escherichia coli isolated from the faeces of healthy humans and cattle. J Med Microbiol 53(10):959–964. https://doi.org/10.1099/jmm.0.45674-0 PubMed DOI

Gordon DM (1997) The genetic structure of Escherichia coli populations in feral house mice. Microbiology 143(6):2039–2046. https://doi.org/10.1099/00221287-143-6-2039 PubMed DOI

Gordon DM (2004) The influence of ecological factors on the distribution and the genetic structure of Escherichia coli. EcoSal Plus 1(1). https://doi.org/10.1128/ecosalplus.6.4.1

Gordon DM, O’Brien CL, Pavli P (2015) Escherichia coli diversity in the lower intestinal tract of humans. Environ Microbiol Rep 7(4):642–648. https://doi.org/10.1111/1758-2229.12300 PubMed DOI

Johnson TJ, Wannemuehler YM, Nolan LK (2008) Evolution of the iss gene in Escherichia coli. Appl Environ Microbiol 74(8):2360–2369. https://doi.org/10.1128/AEM.02634-07 PubMed DOI PMC

Jousset AB, Bernabeu S, Bonnin RA, Creton E, Cotellon G, Sauvadet A, Naas T, Dortet L (2019) Development and validation of a multiplex polymerase chain reaction assay for detection of the five families of plasmid-encoded colistin resistance. Int J Antimicrob Agents 53(3):302–309. https://doi.org/10.1016/j.ijantimicag.2018.10.022 PubMed DOI

Kong RYC, Dung WF, Vrijmoed LLP, Wu RSS (1995) Co-detection of three species of water-borne bacteria by multiplex PCR. Mar Pollut Bull 31(4–12):317–324. https://doi.org/10.1016/0025-326X(95)00139-E DOI

Lorenz SC, Son I, Maounounen-Laasri A, Lin A, Fischer M, Kase JA (2013) Prevalence of hemolysin genes and comparison of ehxA subtype patterns in Shiga toxin-producing Escherichia coli (STEC) and non-STEC strains from clinical, food, and animal sources. Appl Environ Microbiol 79(20):6301–6311. https://doi.org/10.1128/AEM.02200-13 PubMed DOI PMC

Maurelli AT (2007) Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267(1):1–8. https://doi.org/10.1111/j.1574-6968.2006.00526.x PubMed DOI

McLellan SL, Daniels AD, Salmore AK (2003) Genetic characterization of Escherichia coli populations from host sources of fecal pollution by using DNA fingerprinting. Appl Environ Microbiol 69(5):2587–2594. https://doi.org/10.1128/AEM.69.5.2587-2594.2003 PubMed DOI PMC

Meng QM, Wang SH, Han XG, Han Y, Ding C, Dai JJ, Yu SQ (2014) Multiplex PCR assay for detection of virulence genes in avian pathogenic Escherichia coli. Acta Microbiologica Sinica 54(6);696–702. https://doi.org/10.13343/j.cnki.wsxb.2014.06.013 (in China)

Naylor SW, Low JC, Besser TE, Mahajan A, Gunn GJ, Pearce MC, McKendrick IJ, Smith DGE, Gally DL (2003) Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71(3):1505–1512. https://doi.org/10.1128/IAI.71.3.1505-1512.2003 PubMed DOI PMC

Paudel S, Stessl B, Hess C, Zloch A, Hess M (2016) High genetic diversity among extraintestinal Escherichia coli isolates in pullets and layers revealed by a longitudinal study. BMC Vet Res 12(1):221–233. https://doi.org/10.1186/s12917-016-0859-5 PubMed DOI PMC

Pourbakhsh SA, Boulianne M, Martineau-Doizé B, Fairbrother JM (1997) Virulence mechanisms of avian fimbriated Escherichia coli in experimentally inoculated chickens. Vet Microbiol 58(2–4):195–213. https://doi.org/10.1016/s0378-1135(97)00163-6 PubMed DOI

Ren Q, Liao GH, Wu ZH, Lv JF, Chen W (2020) Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang. China J Dairy Sci 103(4):3368–3380. https://doi.org/10.3168/jds.2019-17420 PubMed DOI

Sáenz Y, Briñas L, Domínguez E, Ruiz J, Zarazaga M, Vila J, Torres C (2004) Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrob Agents Chemother 48(10):3996–4001. https://doi.org/10.1128/AAC.48.10.3996-4001.2004 PubMed DOI PMC

Schierack P, Römer A, Jores J, Kaspar H, Guenther S, Filter M, Eichberg J, Wieler LH (2009) Isolation and characterization of intestinal Escherichia coli clones from wild boars in Germany. Appl Environ Microbiol 75(3):695–702. https://doi.org/10.1128/AEM.01650-08 PubMed DOI

Shabana II, Al-Enazi AT (2020) Investigation of plasmid-mediated resistance in E. coli isolated from healthy and diarrheic sheep and goats. Saudi J Biol Sci 27(3);788–796. https://doi.org/10.1016/j.sjbs.2020.01.009

Tello M, Ocejo M, Oporto B, Hurtado A (2020) Prevalence of cefotaxime-resistant Escherichia coli isolates from healthy cattle and sheep in northern Spain: phenotypic and genome-based characterization of antimicrobial susceptibility. Appl Environ Microbiol 86(15):e00742-e820. https://doi.org/10.1128/AEM.00742-20 PubMed DOI PMC

Wada K, Kariyama R, Mitsuhata R, Uehara S, Watanabe T, Monden K, Kumon H (2009) Experimental and clinical studies on fluoroquinolone-insusceptible Escherichia coli isolated from patients with urinary tract infections from 1994 to 2007. Acta Med Okayama 63(5);263–272. https://doi.org/10.18926/AMO/31836

Wang SH, Shi ZY, Xia YJ, Li HQ, Kou YH, Bao YL, Dai JJ, Lu CP (2012) IbeB is involved in the invasion and pathogenicity of avian pathogenic Escherichia coli. Vet Microbiol 159(3–4):411–419. https://doi.org/10.1016/j.vetmic.2012.04.015 PubMed DOI

Wang Y, Kim KS (2002) Role of OmpA and IbeB in Escherichia coli K1 invasion of brain microvascular endothelial cells in vitro and in vivo. Pediatr Res 51(5):559–563. https://doi.org/10.1203/00006450-200205000-00003 PubMed DOI

Whittam TS (1989) Clonal dynamics of Escherichia coli in its natural habitat. Antonie Van Leeuwenhoek 55(1):23–32. https://doi.org/10.1007/bf02309616 PubMed DOI

Zhang YX, Han XG, Zuo JK, Gong JS, Han Y, Fan GB, Wang SH, Tian MX, Ding C, Qi KZ, Yu SQ (2015) Distribution of lipopolysaccharide core type in avian pathogenic Escherichia coli and its correlation with virulence gene. Microbiol China 42;1619–1625. https://doi.org/10.13344/j.microbiol.china.140823 (in China)