Co esponding au ho : Muhsin AYDIN
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Molecula Cha ac e iza ion o An imic obial Resis ance Genes in P ocessed Red Mea -
De i ed Esche ichia coli Isola es
Sehe SAYGI 1 and Muhsin AYDIN 2, *
1 Depa men o Biology, G adua e Educa ion Ins i u e, Adıyaman Uni e si y, Adıyaman, 02040, Tü kiye.
2 Depa men o Biology, Facul y o A s and Science, Adıyaman Uni e si y, Adıyaman, 02040, Tü kiye.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
Publica ion his o y: Recei ed on 19 Sep embe 2025; e ised on 25 Oc obe 2025; accep ed on 27 Oc obe 2025
A icle DOI: h ps://doi.o g/10.30574/gscbps.2025.33.1.0416
Abs ac
This s udy aimed o de e mine he p esence o ex ended-spec um β-lac amase (ESBL) genes (blade, blush, bloa , blas -
M), sul onamide esis ance genes (sul1, sul2, and sul3), and in eg in genes (in 1, in 2, and in 3) in Esche ichia coli isola es
isola ed om p ocessed ed mea samples collec ed in Adıyaman P o ince, Tü kiye. A o al o 14 E. coli isola es we e
analyzed using a molecula echnique. PCR esul s e ealed ha se e al isola es ca ied mul iple esis ance genes
simul aneously. Isola es ha bo ing bo h ESBL and sul onamide esis ance genes we e iden i ied as 19B, 16B, 15B, and
2B, while hose ca ying in eg in and sul onamide esis ance genes we e 14A, 19A, 19B, 13A, and 15B. Only isola es 19B
and 15B con ained all h ee gene g oups. These indings indica e ha oodbo ne E. coli s ains may possess mul iple
an ibio ic esis ance mechanisms, posing a po en ial public heal h isk. The s udy highligh s he impo ance o
implemen ing molecula su eillance p og ams o moni o an ibio ic esis ance wi hin he ood sa e y amewo k.
Keywo ds: Esche ichia coli; An ibio ic Resis ance; ESBL; Sul onamide; In eg in
1. In oduc ion
The widesp ead and uncon olled use o an ibio ics has accele a ed he dissemina ion o esis ance genes among
bac e ia, leading o a se ious global public heal h issue [1]. An imic obial esis ance (AMR) is no longe con ined o
hospi al en i onmen s bu has sp ead ac oss he en i onmen , li es ock p oduc ion, and he ood chain [2]. The use o
an ibio ics as p ophylac ic o g ow h-p omo ing agen s in animal husband y con ibu es o he eme gence o esis an
bac e ial s ains. These bac e ia can be ansmi ed o humans ia ood and cause in ec ions ha a e di icul o ea
[3].
Esche ichia coli is a commensal bac e ium na u ally ound in he in es inal lo a o humans and animals. Howe e ,
ce ain E. coli s ains ha e acqui ed gene ic de e minan s ha enable hem o esis mul iple classes o an ibio ics.
Ex ended-spec um β-lac amases (ESBLs) hyd olyze β-lac am an ibio ics, such as cephalospo ins and monobac ams,
he eby educing he e ec i eness o ea men . Consequen ly, ESBL-p oducing E. coli s ains ha e become impo an
pa hogens in bo h communi y-acqui ed and oodbo ne in ec ions [4].
Resis ance o sul onamide an ibio ics is p ima ily media ed by sul genes (sul1, sul2, and sul3), which a e o en loca ed
on mobile gene ic elemen s such as plasmids and ansposons, allowing ho izon al gene ans e among bac e ial
popula ions [5]. Simila ly, in eg ins a e gene ic s uc u es capable o cap u ing and ans e ing esis ance gene
casse es, playing a majo ole in he dissemina ion o an ibio ic esis ance genes [6].
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
301
Recen s udies ha e epo ed he simul aneous p esence o mul iple esis ance genes in oodbo ne E. coli isola es. This
co-occu ence inc eases he po en ial ansmission o esis an bac e ia h ough he ood chain, posing a signi ican
h ea o public heal h [7].
The aim o his s udy was o in es iga e he p esence and co-occu ence o ESBL, sul onamide esis ance, and in eg on
genes in E. coli isola es ob ained om p ocessed ed mea samples in Adıyaman P o ince, Tü kiye. The indings o his
esea ch will con ibu e o he unde s anding o an ibio ic esis ance mechanisms in oodbo ne bac e ia and suppo
egional an imic obial esis ance moni o ing e o s.
2. Ma e ials and Me hods
2.1. Samples and Isola ion o E. coli S ains
In his s udy, geno ypic iden i ica ion and molecula cha ac e iza ion o Esche ichia coli s ains isola ed om p ocessed
ed mea samples we e conduc ed. A o al o 14 ed mea samples we e analyzed. All samples we e asep ically collec ed
in s e ile polye hylene bags, anspo ed unde cold-chain condi ions, and p ocessed wi hin 2–4 hou s o collec ion o
minimize bac e ial o e g ow h. Fo bac e ial isola ion, 25 g o each mea sample was homogenized in 225 mL o
phospha e-bu e ed saline (PBS, pH 7.6) using a s omache homogenize . Aliquo s o 100 µL om app op ia e dilu ions
we e pla ed on o MacConkey aga and Eosin Me hylene Blue (EMB) aga media. The inocula ed pla es we e incuba ed
a 37°C o 18–24 hou s unde ae obic condi ions. A e incuba ion, colonies wi h ypical E. coli mo phology we e
iden i ied based on hei cha ac e is ic appea ance—pink o ed colonies on MacConkey aga and me allic g een sheen
colonies on EMB aga . Rep esen a i e colonies we e epea edly sub cul u ed o ob ain pu e isola es, which we e
p ese ed a −20°C o molecula analyses.
2.2. DNA Ex ac ion
Genomic DNA was ex ac ed om he con i med E. coli isola es using he boiling me hod. B ie ly, bac e ial colonies we e
suspended in nuclease- ee wa e , hea ed a 95°C o 10 minu es, and cen i uged. The supe na an con aining DNA was
collec ed and s o ed a −20°C un il u he use as a PCR empla e.
2.3. Molecula Con i ma ion o E. coli (uspA Gene)
Molecula con i ma ion o pheno ypically iden i ied isola es was pe o med by polyme ase chain eac ion (PCR) as
sugges ed by Chen and G i i hs (1998) [8] a ge ing he spa gene, which encodes a uni e sal s ess p o ein speci ic o
E. coli. The e e ence s ain E. coli ATCC 25922 was used as a posi i e con ol.
PCR condi ions we e adap ed om he me hod desc ibed by Chen and G i i hs (1998) and op imized o he p esen
s udy. Reac ion mix u es and he mal cycling pa ame e s ollowed a s anda d PCR p o ocol. PCR p oduc s we e
analyzed by 1.5% aga ose gel elec opho esis and isualized unde a UV ansillumina o . Samples yielding an amplicon
o 884 bp we e conside ed molecula ly con i med as E. coli.
2.4. PCR Analysis o Resis ance Genes
Ten a ge genes we e in es iga ed by polyme ase chain eac ion (PCR), including ESBL genes (blaCTX-M, blaSHV, blaOXA,
and blaTEM), sul onamide esis ance genes (sul1, sul2, and sul3), and in eg on class genes (in 1, in 2, and in 3). PCR
eac ions we e pe o med in a o al olume o 25 µL, and he speci ic he mal cycling condi ions o each gene a e
summa ized in Table 3.4. Each eac ion mix u e con ained Mas e Mix, o wa d and e e se p ime s, empla e DNA, and
nuclease- ee wa e .
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
302
Table 1 PCR ampli ica ion condi ions and e e ences o a ge genes used in E. coli isola es
Ta ge
Gene
Ini ial
Dena u a ion
(°C/min)
Dena u a ion
(°C/s)
Annealing
(°C/s)
Ex ension
(°C/s)
No. o
Cycles
Final
Ex ension
(°C/min)
Re e ence
blaTEM
94 / 5
94 / 30
55 / 30
72 / 45
35
72 / 7
[9]
blaSHV
94 / 5
94 / 30
56 / 30
72 / 45
35
72 / 7
blaOXA
94 / 5
94 / 30
52 / 30
72 / 45
35
72 / 7
blaCTX-M
94 / 5
94 / 30
60 / 30
72 / 45
35
72 / 7
sul1
94 / 5
94 / 30
58 / 30
72 / 45
35
72 / 7
[10]
sul2
94 / 5
94 / 30
55 / 30
72 / 45
35
72 / 7
sul3
94 / 5
94 / 30
54 / 30
72 / 45
35
72 / 7
in 1
94 / 5
94 / 30
56 / 30
72 / 45
35
72 / 7
[11]
in 2
94 / 5
94 / 30
57 / 30
72 / 45
35
72 / 7
in 3
94 / 5
94 / 30
58 / 30
72 / 45
35
72 / 7
All PCR eac ions we e pe o med in 25 µL olumes using gene-speci ic p ime s unde he condi ions desc ibed abo e.
2.5. Aga ose Gel Elec opho esis
PCR p oduc s we e sepa a ed on a 1.5% aga ose gel p epa ed in 1X TBE bu e , s ained wi h e hidium b omide, and
isualized using a Vile Lu ma UV gel documen a ion sys em. A 100 bp DNA ladde was used as a molecula ma ke .
2.6. S a is ical Analysis
The da a we e analyzed desc ip i ely, and gene dis ibu ion equencies we e exp essed as pe cen ages.
3. Resul s and Discussion
3.1. De ec ion o ESBL Genes
The molecula analysis o ex ended-spec um β-lac amase (ESBL) gene a ian s in E. coli isola es ob ained om
p ocessed ed mea samples demons a ed a limi ed dis ibu ion o β-lac amase genes. Among he 14 isola es analyzed,
he blaCTX-M gene was de ec ed in only one isola e (15B), whe eas he bloa gene was iden i ied in i e isola es (15A, 19B,
21A, 16B, and 2B). No ampli ica ion was obse ed o he blaTEM and blaSHV genes. The o e all dis ibu ion o he ESBL
genes de ec ed in E. coli isola es is summa ized in Table 2. Rep esen a i e aga ose gel elec opho esis images showing
PCR ampli ica ion o he blaOXA and blaCTX-M genes a e p esen ed in Figu e 1.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
303
Table 2 Dis ibu ion o ESBL genes in E. coli isola es
Numbe
Isola e Code
blaCTX-M
blaOXA
blaSHV
blaTEM
1
18
-
-
-
-
2
13B
-
-
-
-
3
15A
-
+
-
-
4
14A
-
-
-
-
5
19A
-
-
-
-
6
19B
-
+
-
-
7
9B
-
-
-
-
8
13A
-
-
-
-
9
21A
-
+
-
-
10
12B
-
-
-
-
11
19D
-
-
-
-
12
16B
-
+
-
-
13
15B
+
-
-
-
14
2B
-
+
-
-
Figu e 1 Aga ose gel elec opho esis image showing PCR p oduc s o blaOXA, blaTEM, and blaCTX-M genes
The de ec ion o blaOXA in i e isola es and blaCTX-M in a single isola e indica es a ela i ely low p e alence o ESBL-
p oducing E. coli s ains in he analyzed mea samples. The absence o blaTEM and blaSHV genes sugges s ha hese olde
ESBL a ian s may be g adually eplaced by newe β-lac amase ypes such as blaCTX-M and blaOXA in his geog aphical
egion.
When compa ed wi h da a om o he coun ies, no able di e ences can be obse ed. In India, blaCTX-M and blaTEM we e
p edominan among ESBL-posi i e E. coli s ains isola ed om s ee oods, de ec ed in 69.04% and 66.66% o isola es,
espec i ely, while blaOXA was ound in 19.04% and blaSHV was absen [12]. In Ge many, 10.1% o ed mea isola es
ca ied blaCTX-M, whe eas blaSHV and blaTEM we e de ec ed a lowe equencies (2.0% and 0.8%, espec i ely) [13].
Simila ly, s udies in Taiwan epo ed blaCTX-M as he dominan ESBL gene among mul id ug- esis an E. coli s ains om
bo ine ca casses [14], whe eas in Mexico, blaCTX-M was de ec ed in 20% o e ail mea isola es, wi h no de ec ion o
blaTEM, blaSHV, o blaOXA [15]. In addi ion, a s udy conduc ed in he no he n egions o Egyp epo ed ha among E. coli
isola es ob ained om aw bee and mu on, blaTEM, blaCTX-M, and blaOXA genes we e de ec ed in 52.4%, 42.9%, and 14.3%
o isola es, espec i ely [16]. Compa ed wi h hese esul s, he p esen s udy showed a ma kedly lowe p e alence o
ESBL genes, sugges ing geog aphical a ia ions in an ibio ic usage and esis ance dissemina ion pa e ns ac oss
neighbo ing Medi e anean egion.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
304
The p edominance o blaOXA o e blaCTX-M in he p esen s udy may be ela ed o egional di e ences in an ibio ic usage
p ac ices, li es ock managemen , and en i onmen al selec ion p essu es in Tü kiye. The ela i ely low o e all ESBL
de ec ion a e may also e lec limi ed use o hi d-gene a ion cephalospo ins in local animal a ming o di e ences in
sample ype and size.
The iden i ica ion o blaOXA and blaCTX-M posi i e E. coli isola es, e en a low equency, is o pa icula conce n, as hese
genes a e o en plasmid-media ed and can sp ead apidly among bac e ial popula ions ia ho izon al gene ans e [17].
These indings highligh he need o con inuous su eillance o an imic obial esis ance in oodbo ne bac e ia and
emphasize he impo ance o p uden an ibio ic use in li es ock p oduc ion o minimize he isk o dissemina ion o
humans h ough he ood chain.
3.2. De ec ion and Discussion o Sul onamide Resis ance Genes
The molecula sc eening o sul onamide esis ance genes (sul1, sul2, and sul3) among E. coli isola es ob ained om
p ocessed ed mea samples e ealed a iable gene dis ibu ions. As shown in Table 3, he sul1 gene was de ec ed in
isola es 19A, 13A, and 12B; sul2 was iden i ied in isola es 18, 13B, 14A, 19A, 19B, 13A, 12B, 16B, and 2B; and sul3 was
de ec ed in isola es 18, 14A, and 15B. Rep esen a i e aga ose gel elec opho esis images o sul1/sul2 and sul3
ampli ica ion p oduc s a e p esen ed in Figu es 2 and 3, espec i ely.
Table 3 Dis ibu ion o sul Genes in E. coli Isola es
Numbe
Isola e
Code
sul1
sul2
sul3
1
18
-
+
+
2
13B
-
+
-
3
15A
-
-
-
4
14A
-
+
+
5
19A
+
+
-
6
19B
-
+
-
7
9B
-
-
-
8
13A
+
+
-
9
21A
-
-
-
10
12B
+
+
-
11
19D
-
-
-
12
16B
-
+
-
13
15B
-
-
+
14
2B
-
+
-
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
305
Figu e 2 Aga ose gel elec opho esis showing ampli ica ion o sul1 and sul2 genes in E. coli isola es
Figu e 3 Aga ose gel elec opho esis showing ampli ica ion o sul3 gene in E. coli isola es
Mul iple gene combina ions we e obse ed in se e al isola es. Speci ically, sul1 and sul2 coexis ed in isola es 13A, 19A,
and 12B, while sul2 and sul3 we e simul aneously de ec ed in isola es 18 and 14A. These esul s indica e ha some E.
coli s ains may ca y mul iple sul onamide esis ance de e minan s, po en ially enhancing hei abili y o su i e unde
selec i e an ibio ic p essu e.
When compa ed wi h esul s epo ed om o he coun ies, no iceable a ia ions in sul gene dis ibu ion pa e ns can
be obse ed. In Spain, Ramos e al. epo ed ha among E. coli s ains isola ed om po k mea , 23.1% ha bo ed bo h
sul1 and sul2 genes, 3.1% ca ied sul2 and sul3, and 1.5% ca ied sul1 and sul3 oge he ; no ably, only one isola e
con ained all h ee sul genes simul aneously [18]. In Canada, a s udy in es iga ing E. coli isola es om a comme cial
bee p ocessing plan ound ha sul1 was p esen in samples om hides (6%), washed ca casses (20%), con eyo bel s
(7%), bee immings (15%), and g ound bee (4%), whe eas sul2 was de ec ed in 9%, 10%, 12%, 4%, and 15% o hese
espec i e sample ypes, and no isola es ca ied sul3 [19]. Simila ly, an Aus ian s udy analyzing E. coli om mul iple
mea sou ces (po k, bee , poul y, and minced mea ) ound ha among 142 sul onamide- esis an isola es, sul2 (n =
113) was a mo e p e alen han sul1 (n = 32), wi h only h ee isola es ca ying bo h genes [20].
The indings o he p esen s udy a e consis en wi h hese in e na ional epo s, as sul2 was also he mos equen ly
de ec ed gene, ollowed by sul1 and sul3. The de ec ion o mul iple sul genes in indi idual isola es sugges s he po en ial
o ho izon al gene ans e and co-selec ion mechanisms unde an ibio ic p essu e. The ela i ely lowe de ec ion a e
o sul3 compa ed wi h sul1 and sul2 aligns wi h p e ious obse a ions ha sul3 is a less common a ian , o en es ic ed
o speci ic plasmid ypes o ecological niches.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
306
O e all, hese esul s highligh he pe sis en p esence o sul onamide esis ance de e minan s in oodbo ne E. coli and
unde sco e he necessi y o ongoing moni o ing o assess hei ole in he b oade dissemina ion o an imic obial
esis ance wi hin he ood chain.
3.3. De ec ion and Discussion o In eg in Genes
The molecula sc eening o E. coli isola es ob ained om p ocessed ed mea samples e ealed he p esence o he in 1
gene, whe eas in 2 and in 3 we e no de ec ed in any o he samples. As shown in Table 4, he in 1 gene was iden i ied
in isola es 18, 14A, 19A, 19B, 13A, and 15B. Rep esen a i e aga ose gel elec opho esis images showing PCR
ampli ica ion o he in 1 gene a e p esen ed in Figu e 4.
Table 4 Dis ibu ion o in 1, in 2, and in 3 genes among E. coli isola es ob ained om p ocessed ed mea samples
Numbe
Isola e Code
in 1
in 2
in 3
1
18
+
-
-
2
13B
-
-
-
3
15A
-
-
-
4
14A
+
-
-
5
19A
+
-
-
6
19B
+
-
-
7
9B
-
-
-
8
13A
+
-
-
9
21A
-
-
-
10
12B
-
-
-
11
19D
-
-
-
12
16B
-
-
-
13
15B
+
-
-
14
2B
-
-
-
Figu e 4 Aga ose gel elec opho esis showing ampli ica ion o he in 1 gene in E. coli isola es
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
307
The de ec ion o in 1 in 6 o he 14 isola es indica es ha class 1 in eg ons a e p esen among E. coli s ains isola ed
om p ocessed mea p oduc s, while he absence o in 2 and in 3 genes sugges s limi ed dissemina ion o hese in eg on
classes in he analyzed samples. In eg ons play a key ole in he ho izon al ans e o an ibio ic esis ance genes, and
he iden i ica ion o in 1-posi i e isola es highligh s hei po en ial ole in he sp ead o mul id ug esis ance
de e minan s.
Simila obse a ions ha e been epo ed in p e ious s udies conduc ed in di e en geog aphical egions. In No way,
class 1 and class 2 in eg ons we e de ec ed in 12% (in 1) and 6% (in 2) o 241 esis an E. coli s ains isola ed om
mea p oduc s, espec i ely [21]. In con as , a s udy conduc ed in Sou h Ko ea iden i ied class 1 in eg ons (in 1) in 16
isola es om animal-de i ed oods, while class 2 and class 3 in eg ons we e no de ec ed, consis en wi h he indings
o he p esen s udy [22]. Likewise, in India, 56 o 96 (58.3%) mul id ug- esis an E. coli isola es om eady- o-ea ood
samples we e posi i e o class 1 in eg ons, showing a signi ican co ela ion be ween in eg on occu ence and ood
o igin [23].
Taken oge he , hese esul s indica e ha he p esence o class 1 in eg ons in E. coli isola es om mea p oduc s is a
globally obse ed phenomenon, al hough hei p e alence a ies by coun y and sample ype. The de ec ion o in 1 in
his s udy, e en a a mode a e equency, sugges s ha p ocessed mea p oduc s may ac as ese oi s o in eg on-
associa ed esis ance genes. Con inuous moni o ing o in eg on-bea ing E. coli isola es is he e o e essen ial o be e
unde s and hei ole in he dissemina ion o an imic obial esis ance h ough he ood chain.
3.4. O e all E alua ion
The combined e alua ion o ESBL, sul onamide, and in eg on gene p o iles e ealed a clea indica ion o mul id ug
esis ance among E. coli isola es ob ained om p ocessed mea samples. Al hough he o e all de ec ion equency o
indi idual genes was ela i ely low, se e al isola es ha bo ed mul iple esis ance de e minan s simul aneously,
sugges ing he p esence o mobile gene ic elemen s media ing ho izon al gene ans e .
The p edominance o blaOXA and sul2 genes, oge he wi h in 1-posi i e isola es, highligh s he po en ial linkage be ween
β-lac amase, sul onamide, and in eg on-associa ed esis ance mechanisms. Such co-localiza ion inc eases he isk o
mul id ug esis ance dissemina ion h ough he ood chain.
These indings unde line he impo ance o in eg a ed molecula su eillance s a egies ha simul aneously a ge
ESBLs, sul genes, and in eg on classes o p o ide a mo e comple e unde s anding o an imic obial esis ance dynamics
in oodbo ne E. coli.
4. Conclusion
This s udy p o ides a comp ehensi e molecula cha ac e iza ion o Esche ichia coli isola es ob ained om p ocessed
ed mea samples, ocusing on β-lac amase (ESBL), sul onamide esis ance, and in eg on genes. The de ec ion o blaOXA
and blaCTX-M genes, along wi h he widesp ead occu ence o sul2 and he p esence o class 1 in eg ons (in 1), indica es
ha oodbo ne E. coli s ains may ac as ese oi s o mul iple esis ance de e minan s. The coexis ence o hese genes
in ce ain isola es sugges s possible plasmid-media ed ho izon al gene ans e e en s con ibu ing o he
dissemina ion o mul id ug esis ance wi hin he ood chain. Al hough he o e all gene p e alence was mode a e, hese
indings highligh he need o con inuous molecula su eillance o moni o he sp ead o an imic obial esis ance.
S eng hening hygiene s anda ds, egula ing an ibio ic use in animal husband y, and implemen ing in eg a ed
esis ance moni o ing sys ems a e c ucial s eps o p e en u he dissemina ion o esis an E. coli om ood sou ces
o humans.
Compliance wi h e hical s anda ds
Acknowledgemen s
This s udy was suppo ed by The Scien i ic and Technological Resea ch Council o Tü kiye (TÜBİTAK) 2209-A p og am,
P ojec No: 1919B012401787.
Disclosu e o con lic o in e es
No con lic o in e es o be disclosed.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 300-309
308
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