The Phylogenetic Structure of Reptile, Avian and Uropathogenic Escherichia coli with Particular Reference to Extraintestinal Pathotypes
Abstract
:1. Introduction
2. Results
2.1. Phylogenetic Groups of E. coli
2.2. Virulence Gene Typing
2.3. Analysis of Phylogenetic Relationships between E. coli Strains from Different Hosts
2.4. Multi-Locus Sequence Typing
3. Discussion
4. Materials and Methods
4.1. Bacterial Strains
4.2. Isolation and Identification of Bacterial Strains
4.3. DNA Extraction
4.4. Phylogenetic Groups of E. coli
4.5. Virulence Genotyping
4.6. Gel Electrophoresis of PCR Amplification Products
4.7. Restriction Analysis Combined with Pulsed-Field Gel Electrophoresis (RAE-PFGE)
4.8. Genetic Population Structure Analysis of E. coli Strains by Multi-Locus Sequence Typing
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Group of Escherichia coli Strains | |||||
---|---|---|---|---|---|
RepEC | UPEC | APEC | |||
Strain Code | Source of Isolated Bacteria | Strain Code | Source of Isolated Bacteria | Strain Code | Source of Isolated Bacteria |
Escherichia coli strains isolated from feces of reptiles (snakes, lizards and turtles) | Escherichia coli isolated from urine samples of patients with symptomatic and asymptomatic urinary tract infections | Escherichia coli strains isolated from extraintestinal organs (heart, liver) of poultry with colibacillosis | |||
200E | Snake (Lamprophis fuliginosus) | 15641.38 | 46A | ||
201E | Snake (Orthriophis taeniurus) | 15514.33 | 1316 | ||
203E | Lizard (Pogona vitticeps) | 15165.15 | 1422B | ||
204E | Lizard (Chamaeleo calyptratus) | 15279.21 | 1442A | ||
205E | Lizard (Anolis barbatus) | 15988.54 | 1288 | ||
206E | Snake (Epicrates cenchria) | 15300.22 | 189A | ||
207E | Snake (Lamprophis fuliginosus) | 15593.39 | 36C | ||
208E | Snake (Lamprophis fuliginosus) | 15159.19 | 1453 | ||
209E* | Snake (Lamprophis fuliginosus) | 15607.35 | 172A | ||
210E | Snake (Lampropeltisgetula) | 15992.42 | 188 | ||
211E | Snake (Elaphe schrencki) | 15997.9 | 1410 | ||
212E | Snake (Coelognathus radiata) | 15550.25 | 1451 | ||
305C | Turtle (Kinixys belliana) | 15589.37 | 1251B | ||
213E | Turtle (Chelonoidis nigra) | 1110 | 06B | ||
220E | Turtle (Geochelone platynota) | 15599.34 | 1386C | ||
222E | Turtle (Testudo marginata) | 15067.4 | 17A | ||
226E | Lizard (Chamaeleo calyptratus) | 15059.6 | 60C | ||
228E | Turtle (Geochelone platynota) | 15320.27 | 240 | ||
229E | Turtle (Astrochelysradiata) | 15038.2 | 73C | ||
230E | Turtle (Centrochelys sulcata) | 1119 | 010A | ||
234E | Turtle (Testudo horsfieldii) | 15611.41 | 169 | ||
239E | Snake (Lampropeltis triangulum) | 15155.16 | 1216 | ||
240E | Lizard (Anolis baracoae) | 15035.8 | 1326B | ||
241E | Turtle (Chelonoidisnigra) | 15084.1 | 1239 |
Gene | Sequences of Primers | PCR Product Size (bp) | Gene Bank ID |
---|---|---|---|
yjaA | 5′-CAAACGTGAAGTGTCAGGAG-3′ 5′-AATGCGTTCCTCAACCTGTG-3′ | 288 | 948515 |
chuA | 5′-CAAACGTGAAGTGTCAGGAG-3′ 5′-AATGCGTTCCTCAACCTGTG-3′ | 211 | 7155958 |
TspE4C2 | 5′-CACTATTCGTAAGGTCATCC-3′ 5′-AGTTTATCGCTGCGGGTCGC-3′ | 152 | EU240725.1 |
arpA | 5′-AACGCTATTCGCCAGCTTGC-3′ 5′-TCTCCCCATACCGTACGCTA-3′ | 400 | 7155679 |
arpA | 5′-GATTCCATCTTGTCAAAATATGCC-3′ 5′-GAAAAGAAAAAGAATTCCCAAGAG-3′ | 301 | 944933 |
trpA | 5′-AGTTTTATGCCCAGTGCGAG-3′ 5′-TCTGCGCCGGTCACGCCC-3′ | 219 | 912862 |
trpA | 5′-CGGCGATAAAGACATCTTCAC-3′ 5′-GCAACGCGGCCTGGCGGAAG-3′ | 489 | 13702525 |
Gene | Sequences of Primers | PCR Product Size (bp) | Gene Bank ID | Biological (Enzymatic) Function |
---|---|---|---|---|
astA | 5′-CCATCAACACA-3′ 5′-TCAGGTCGCGAGTG-3′ | 116 | AF143819 | Gene encoding heat-stable toxin 1 (ST1) |
Iss | 5′-ATCACATAGGATTCTGCCG-3′ 5′-CAGCGGAGTATAGATGCCA-3′ | 309 | X52665 | Gene encoding outer membrane protein of increased serum survival |
irp2 | 5′-GGATTCGCTGTTACCGGAC3′ 5′-AACTCCTGATACAGGTGGC-3′ | 413 | L18881 | Gene encoding iron binding protein |
iucD | 5′-ACAAAAAGTTCTATCGCTTCC-3′ 5′-CCTGATCCAGATGATGCTC-3′ | 714 | M18968 | Gene encoding siderophore’s complex |
tsh | 5′-ACTATTCTCTGCAGGAAGTC-3′ 5′-TTCCGATGTTCTGAA-3′ | 824 | AF218073 | Gene encoding thermolabile haemagglutinin |
vat | 5′-TCCTGGGACATAATGGTCAG-3′ 5′- GTGTCAGAACGGAATTGT-3′ | 981 | AY151282 | Gene encoding vacuolating autotransporter toxin |
fyuA | 5′-TGATTAACCCCGCGACGGGAA-3′ 5′-CGCAGTAGGCACGATGTTGTA-3′ | 880 | Z38064 | Gene belonging to the operon encoding aerobactin siderophore complex at the plasmid ColV-K30 |
stx2f | 5′-ATCCTATTCCCGGGAGTTTACG-3′ 5′-GCGTCATCGTATACACAGGAGC-3′ | 338 | 912579 | Gene encoding Shiga like toxin |
hlyE | 5′-GGTGCAGCAGAAAAAGTTGTAG-3′ 5′-TCTCGCCTGATAGTGTTTGGTA-3′ | 569 | 13701006 | Gene encoding haemolysin |
fimC | 5′-GTTGATCAAACCGTTCAG-3′ 5′-AATAACGCGCCTGGAACG-3′ | 424 | 948843 | Gene encoding fimbriae type I |
eae | 5′-TCAATGCAGTTCCGTTATCAGTT-3′ 5′-GTAAAGTCCGTTACCCCAACCTG-3′ | 482 | AF022236 | Gene encoding intimin |
bfp | 5′-GGAAGTCAAATTCATGGGGGTAT-3′ 5′-GGAATCAGACGCAGACTGGTAGT 3′ | 246 | KJ020697 | Gene encoding bundle forming pilli |
cvi/cva | 5′-TGGTAGAATGTGCCAGAGCAAG-3′ 5′-GAGCTGTTTGTAGCGAAGCC-3′ | 1181 | AJ223631 | Gene encoding colicin at the ColV plasmid |
papC | 5′-GTGGCAGTATGAGTAATGACCGTTA-3′ 5′-ATATCCTTTCTGCAGGGATGCAATA-3′ | 200 | X61239 | Gene encoding P fimbriae subunit |
kpsMTII | 5′-GCGCATTTGCTGATACTGTTG-3′ 5′-CATCCAGACGATAAGCATGAGCA-3′ | 272 | X53819 | Gene encoding extracellular capsules type II biosynthesis proteins |
kpsMT (K1) | 5′-TAGCAAACGTTCTATTGGTGC-3′ 5′-CATCCAGACGATAAGCATGAGCA-3′ | 153 | M57382 | Gene encoding capsules antigen K1 |
kpsMTIII | 5′-TCCTCTTGCTACTATTCCCCCT -3′ 5′-AGGCGTATCCATCCCTCCTAAC-3′ | 392 | AF007777 | Gene encoding extracellular capsules type III biosynthesis proteins |
rfc | 5′-ATCCATCAGGAGGGGACTGGA-3′ 5′-AACCATACCAACCAATGCGAG -3′ | 788 | U39042 | Gene encoding O-side-chain antigen of LPS |
traT | 5′- GGTGTGGTGCGATGAGCACAG-3′ 5′-CACGGTTCAGCCATCCCTGAG-3′ | 290 | J01769 | Gene encoding serum resistance and pathogenicity-related protein |
Gene | Primer’s Sequences | PCR Product Size (bp) | Biological (Enzymatic) Function |
---|---|---|---|
adk | 5’-ATTCTGCTTGGCGCTCCGGG-3’ 5’-CCGTCAACTTTCGCGTATTT-3’ | 583 | adenylate kinase |
fumC | 5’-TCACAGGTCGCCAGCGCTTC-3’ 5’-GTACGCAGCGAAAAAGATTC-3’ | 806 | fumarate hydratase |
gyrB | 5’-TCGGCGACACGGATGACGGC-3’ 5’-GTCCATGTAGGCGTTCAGGG-3’ | 911 | DNA gyrase |
icd | 5’-ATGGAAAGTAAAGTAGTTGTTCCGGCACA-3’ 5’-GGACGCAGCAGGATCTGTT-3’ | 878 | isocitrate dehydrogenase |
mdh | 5’-AGCGCGTTCTGTTCAAATGC-3’ 5’-CAGGTTCAGAACTCTCTCTGT-3’ | 932 | malate dehydrogenase |
purA | 5’-CGCGCTGATGAAAGAGATGA-3’ 5’-CATACGGTAAGCCACGCAGA-3’ | 816 | adenylosuccinate synthetase |
recA | 5’-ACCTTTGTAGCTGTACCACG-3’ 5’-TCGTCGAAATCTACGGACCGGA-3’ | 780 | ATP/GTP binding motif |
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Group of E. coli | E. coli Strain Code | P | Asigned Sequence Type | Description of STs | Citations |
---|---|---|---|---|---|
UPEC (n = 3) | 15279.21 | D | ST321 | ST321 is characteristic of nonpathogenic E. coli strains isolated from wild animals. | [29] |
1119 | C | ST410 | which includes pathogenic E. coli strains (human UPEC strains, predominantly). | [29,30] | |
15035.8 | B1 | ST12 | ST12 is typical of extraintestinal pathogenic E. coli strains causing systemic infections in warm-blooded animals and also typical of E. coli causing urinary tract infections (UTIs) among humans. | [29,31] | |
APEC (n = 4) | 1288 | B1 | ST1582 | ST1582 is characteristic for UPEC strains causing UTIs in horses. | [29] |
1239 | D | ST665 | ST665 is typical of nonpathogenic E. coli strains isolated from poultry. | [29,32] | |
189A | B2 | ST131 | ST131 is a globally disseminated clone that poses a substantial health risk to humans, causing acute extraintestinal infections, such as serious UTI, urosepsis and sepsis. | [8,29,33,34] | |
60C | ST117 | ST117, which is a heterogenic group of extraintestinal pathogenic E. coli strains. | [29,35] | ||
REPEC (n = 4) | 200E | B1 | ST446 | ST446 is typical of APEC strains and also of other human pathogenic extraintestinal E. coli. | [29,36] |
209E | B2 | ST681 | ST 681 includes E. coli strains pathogenic for humans and other animals. | [29,37] | |
212E | B1 | ST212 | This heterogenous ST mainly includes UPEC strains as well as other pathogenic and nonpathogenic E. coli strains. | [29,38] | |
305C | B1 | New ST! | Strain 305C could not be assigned to any known ST, although it could be a member of the ST88 clonal complex (with differences in two alleles adk and mdh; unconfirmed data). | - |
Percentage Prevalence of VGs | Frequency of VGs |
---|---|
0–10% | Very low |
11–20% | Low |
21–45% | Medium |
46–80% | High |
81–100% | Very high |
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Książczyk, M.; Dudek, B.; Kuczkowski, M.; O’Hara, R.; Korzekwa, K.; Wzorek, A.; Korzeniowska-Kowal, A.; Upton, M.; Junka, A.; Wieliczko, A.; et al. The Phylogenetic Structure of Reptile, Avian and Uropathogenic Escherichia coli with Particular Reference to Extraintestinal Pathotypes. Int. J. Mol. Sci. 2021, 22, 1192. https://doi.org/10.3390/ijms22031192
Książczyk M, Dudek B, Kuczkowski M, O’Hara R, Korzekwa K, Wzorek A, Korzeniowska-Kowal A, Upton M, Junka A, Wieliczko A, et al. The Phylogenetic Structure of Reptile, Avian and Uropathogenic Escherichia coli with Particular Reference to Extraintestinal Pathotypes. International Journal of Molecular Sciences. 2021; 22(3):1192. https://doi.org/10.3390/ijms22031192
Chicago/Turabian StyleKsiążczyk, Marta, Bartłomiej Dudek, Maciej Kuczkowski, Robert O’Hara, Kamila Korzekwa, Anna Wzorek, Agnieszka Korzeniowska-Kowal, Mathew Upton, Adam Junka, Alina Wieliczko, and et al. 2021. "The Phylogenetic Structure of Reptile, Avian and Uropathogenic Escherichia coli with Particular Reference to Extraintestinal Pathotypes" International Journal of Molecular Sciences 22, no. 3: 1192. https://doi.org/10.3390/ijms22031192