Tracing the Evolutionary Pathways of Serogroup O78 Avian Pathogenic Escherichia coli
Abstract
:1. Introduction
2. Results and Discussion
2.1. O78 APEC Strains Identified during 2012–2020
2.2. Modified rpoB Sequence Typing (RSTing) of E. coli Strains
2.3. Hypothetical Evolutionary Pathways of E. coli and O78 APEC Strains
2.4. General Genomic Information of the Six Representative O78 APEC Strains from RST3-1, RST4-4, and RST21-1
2.5. Correlation of Genomic Sequence Coverage/Identity and CRISPR Contents between the Same RSTs Containing Major O78 Strains
E19057 | E123 | APEC O78 | E18005 | E19025 | NCTC11129 | E12049 | E14033 | PSUO78 | |
---|---|---|---|---|---|---|---|---|---|
Accession no. | CP126934.1 | CP126955.1 | CP004009.1 | CP126946.1 | CP126931.1 | LR134222.1 | CP126952.1 | CP126948.1 | CP012112.1 |
Origin | Chicken | Chicken | Turkey | Chicken | Chicken | unknown | Chicken | Chicken | Chicken |
RST | 3-1 | 3-1 | 3-1 | 4-4 | 4-4 | 4-4 | 21-1 | 21-1 | 21-1 |
MLST (Achman) | ST23 | ST369 | ST23 | ST155 | ST155 | ST155 | ST11749 | ST48 | ST5940 |
mPPT | 2-5 | 2-3-4 | 3-4 | 1-2-3-5(2)-6 | 1-2-3(2)-4-5-6 | 2-3-4-5 | 1-2-5 | 1-2-4-5 | 2-4-5-7 |
Serotype | O78:H4 | O78:H4 | O78:H9 | O78:H51 | O78:H51 | O8, O60:H51 | O78:H4 | O78:H4 | O78:H4 |
Total Length (bp) | 4,885,187 | 4,998,625 | 4,798,435 | 5,129,598 | 5,086,337 | 5,008,027 | 5,170,367 | 5,021,334 | 4,988,493 |
GC Content (%) | 50.60% | 50.64% | 50.70% | 50.64% | 50.70% | 50.78% | 50.74% | 50.79% | 50.80% |
No. of CDSs | 4586 | 4690 | 4504 | 4771 | 4751 | 4697 | 4788 | 4658 | 4791 |
No. of rRNA | 22 | 22 | 19 | 21 | 22 | 22 | 22 | 22 | 22 |
No. of tRNA | 86 | 82 | 88 | 92 | 95 | 89 | 97 | 90 | 88 |
No. of CRISPRS | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Coding ratio (%) | 87.30% | 87.10% | 87.60% | 87.00% | 87.20% | 87.10% | 86.80% | 87.20% | 86.60% |
Plasmid 1 a | pEND_Eco19057-1 (CP126935.1) (IncI1-1 (alpha), 100%; 110,406 bp) | pEND_Eco 123-1 (CP126956.1) (IncFIB, 98.39%; 121,788 bp) | 217,830 bp | pEND_Eco 18005 (CP126947.1) (IncFIB, 98.39%; 204,838 bp) | pEND_Eco 19025-1 (CP126932.1) (IncFIB, 98.39%; 160,439 bp) | No data | pEND_Eco 12049-1 (CP126953.1) (IncFIB, 99.12%; 155,857 bp) | pEND_Eco 14033-1 (CP126949.1) (IncFIB, 98.39%; 145,212 bp) | pPSUO78_1 (CP012113.1) (132,464 bp) |
Plasmid 2 | pEND_Eco 19057-2 (CP126936.1) (IncFIB, 98.39%; 104,962 bp) | pEND_Eco 123-2 (CP126957.1) (No hit; 68,426 bp) | 113,260 bp | pEND_Eco 19025-2 (CP126933.1) (IncY, 99.38%; 90,722 bp) | pEND_Eco 12049-2 (CP126954.1) (IncI1-1(alpha), 100%; 114,229 bp) | pEND_Eco 14033-2 (CP126950.1) (IncI1-1 (alpha), 100%; 115,173 bp) | pPSUO78_2 (CP012114.1) (109,613 bp) | ||
Plasmid 3 | pEND_Eco 14033-3 (CP126951.1) (IncFIB (H89-PhagePlasmid), 98.7%; 108,542 bp) | ||||||||
Plasmid 4 | pEND_Eco 14033-4 (CP130557.1) (IncI2(delta), 97.15%; 61,041 bp) | ||||||||
No. Genomic islands (GI) b | 69 | 70 | 47 | 94 | 88 | 61 | 94 | 77 | 80 |
2.6. Evolutionary Linkage between Early-Appearing RSTs
2.7. Evolution of O Serogroups in Different RSTs
2.8. Profiling Virulence Genes of O78 APEC Strains
2.9. Antibiograms of O78 APEC Strains
2.10. Profiles of Microcins and Colicins of O78 APEC Strains
3. Materials and Methods
3.1. Bacterial Strains and Identification
3.2. Serotyping and Phylogrouping of E. coli
3.3. rpoB Sequence Typing (RSTing) and Molecular Prophage Typing (mPPTing)
3.4. Molecular Pathotyping
3.5. Antibiotic Susceptibility Testing and Molecular Profiling of Antibiotic Resistance Genes
3.6. Comparative Genomics
3.7. Identification of Bacteriocin Genes in O78 APEC
3.8. Antimicrobial Activity Test of Bacteriocin
3.9. Statistical Analysis
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Strain | Year of Isolation | Chicken Type a | Age (Day-Old) | Phylo- Group | RST b | No. of Virulence Genes | Strain | Year of Isolation | Chicken Type a | Age (Day-Old) | Phylo- Group | RST | No. of Virulence Genes |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
E12049 | 2012 | KNC | 40 | F | 21-1 | 20 | E16015 | 2016 | B | 24 | B1 | 5-1 | 15 |
E14033 | 2014 | L | 76 | F | 21-1 | 19 | E17039 | 2017 | BB | 263 | B1 | 12-6 | 15 |
E12090 | 2012 | L | 124 | F | 21-1 | 18 | E19033 | 2019 | BB | 134 | B1 | 4-4 | 15 |
E18005 | 2018 | BB | 209 | B1 | 4-4 | 17 | E19057 | 2019 | L | 148 | C | 3-1 | 14 |
E16018 | 2016 | L | 451 | B1 | 4-4 | 16 | E16023 | 2016 | BB | 203 | E | 3-1 | 14 |
E18016 | 2018 | BB | 163 | B1 | 4-4 | 16 | E16039 | 2016 | L | 252 | B1 | 4-4 | 14 |
E18027 | 2018 | B | 2 | E | 21-1 | 16 | E19024 | 2019 | L | 315 | C | 3-1 | 14 |
E19014 | 2019 | BB | 7 | B1 | 4-4 | 16 | E20019 | 2020 | L | 310 | E | 3-1 | 14 |
E19025 | 2019 | B | 7 | B1 | 4-4 | 16 | E17001 | 2017 | BB | 264 | C | 3-1 | 13 |
E19034 | 2019 | BB | 235 | B1 | 4-4 | 16 | E12050 | 2012 | B | 26 | C | 3-1 | 12 |
E19045 | 2019 | L | 19 | B1 | 4-4 | 16 | E13028 | 2013 | BB | 29 | C | 3-1 | 12 |
E19070 | 2019 | BB | 170 | B1 | 4-4 | 16 | E20042 | 2020 | L | 161 | C | 3-1 | 11 |
E12091 | 2012 | BB | 236 | B1 | 4-4 | 15 | E19013 | 2019 | BB | 77 | C | 4-5 | 9 |
E15016 | 2015 | B | 30 | B1 | 4-4 | 15 | E19040 | 2019 | BB | 195 | C | 3-1 | 9 |
E15026 | 2015 | BB | 273 | B1 | 4-4 | 15 | E19056 | 2019 | B | 3 | A | 3-1 | 9 |
E16011 | 2016 | L | 136 | B1 | 4-4 | 15 | E123 | 2003 | NA c | NA | C | 3-1 | 17 |
Pathogenic Bacteria | Strain | Accession No. | Size of rpoB | RST | Identity (%) |
---|---|---|---|---|---|
Corynebacterium diphtheriae | 31A | CP003206.1 | 3531 | ND | ND |
Bacillus anthracis | A2084 | NC_007530.2 | 3534 | ND | ND |
Staphylococcus aureus | PMB81 | CP03444.1 | 3552 | ND | ND |
Listeria monocytogenes | EGD-e | NC_003210.1 | 3555 | ND | ND |
Streptococcus pneumoniae | Hu17 | NZ_CP020549.1 | 3612 | ND | ND |
Enterococcus faecalis | T5 | NZ_KB944666.1 | 3615 | ND | ND |
Clostridium perfringens | CPI 18-6 | NZ_CP075979.1 | 3705 | ND | ND |
Clostridium difficile | s-0253 | NZ_CP076401.1 | 3717 | ND | ND |
Vibrio cholerae | RFB16 | CP043554.1 | 4026 | ND | ND |
Escherichia coli | RST0 | ND a | 4029 | 0 | 100 |
Escherichia fergusonii | RHB10-C04 | CP057918.1 | 4029 | 40 | 99.1 |
Escherichia fergusonii | ATCC 35471 | CP042945.1 | 4029 | 53 | 98.7 |
Escherichia fergusonii | RHB02-C14 | CP055872.1 | 4029 | 60 | 98.5 |
Escherichia albertii | RM10507 | CP043258.1 | 4029 | 69 | 98.3 |
Escherichia albertii | ChinaSP140150 | CP025676.1 | 4029 | 100 | 97.5 |
Escherichia albertii | BIA_36 | CP117590.1 | 4029 | 104 | 97.4 |
Escherichia marmotae | W49-2 | CP093239.1 | 4029 | 106 | 97.4 |
Salmonella enterica serovar Indiana | SI67 | CP050783.1 | 4029 | 177 | 95.6 |
Salmonella bongori | N268-08 | CP006608.1 | 4029 | 251 | 93.8 |
Klebsiella pneumoniae | XH210 | CP052761.1 | 4029 | 259 | 93.6 |
Enterobacter cloacae | colR/S | CP010512.1 | 4029 | 264 | 93.4 |
Serratia marcescens | SmUNAM836 | CP012685.1 | 4029 | 491 | 87.8 |
Yersinia pseudotuberculosis | IP2666pIB1 | CP032566.1 | 4029 | 588 | 85.4 |
Yersinia pestis | FDAARGOS_603 | CP033690.1 | 4029 | 590 | 85.4 |
Proteus mirabilis | 1035 | CP072779.1 | 4029 | 758 | 81.1 |
Pasteurella multocida | FDAARGOS_218 | CP020405.2 | 4029 | 1027 | 74.5 |
Haemophilus influenzae | Hi375 | CP009610.1 | 4032 | ND | ND |
Pseudomonas aeruginosa | PAO1 | AE004091.2 | 4074 | ND | ND |
Acinetobacter baumannii | Ab421_GEIH-2010 | CP014266.1 | 4074 | ND | ND |
Legionella pneumophila | C9 | CP015941.1 | 4107 | ND | ND |
Bordetella bronchiseptica | NCTC10543 | LR134326.1 | 4113 | ND | ND |
Neisseria gonorrheae | AT159 | CP097846.1 | 4179 | ND | ND |
Moraxella catarrhalis | CCRI-195ME | CP018059.1 | 4239 | ND | ND |
RST3-1 | RST4-4 | RST5-1 | RST12-6 | RST21-1 | |
---|---|---|---|---|---|
Frequency out of MDR strains (%) a | 3/18 | 11/18 | 1/18 | 1/18 | 2/18 |
(16.7%) | (61.1%) b | (5.6%) | (5.6%) | (11.1%) | |
MDR Frequency out of each RST (%) | 3/11 | 11/14 | 1/1 | 1/1 | 2/4 |
(27.3%) | (78.6%) | (100%) | (100%) | (50%) |
Antibiotics Resistance- Related Genes | gyrA | tetB | sul2 | blaTEM | blaCTX-M -G1 | strA/strB | tetA | aadA1 /A2 | aac(3)II | sul1 | dfrA1 | blaCTX-M -G9 | ampC | floR | blaSHV |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Frequency (%) | 29 | 16 | 12 | 10 | 9 | 7 | 6 | 6 | 6 | 5 | 4 | 3 | 2 | 2 | 1 |
(90.6) | (50.0) | (37.5) | (31.3) | (28.1) | (21.9) | (18.8) | (18.8) | (18.8) | (15.6) | (12.5) | (9.4) | (6.3) | (6.3) | (3.1) |
Strain | RST | Chromosome | Plasmid | No. of Microcin/Colicin a | |||
---|---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | ||||
E123 | 3-1 | None | Microcin V (Colicin V) | None | 1 | ||
E19057 | 3-1 | None | Colicin Ia | Microcin V (Colicin V) | 2 | ||
E18005 | microcin H47 | Microcin J25 | 4 | ||||
Colicin M | |||||||
4-4 | Microcin V (Colicin V) | ||||||
Colicin B (pseudo) | |||||||
E19025 | None | Microcin J25 | None | 3 | |||
Colicin M | |||||||
4-4 | Microcin V (Colicin V) | ||||||
Colicin B (pseudo) | |||||||
E12049 | 21-1 | None | Colicin M | Colicin Ib | 2 | ||
E14033 | 21-1 | None | None | ColIcin Ib | None | None | 1 |
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Ha, E.-J.; Hong, S.-M.; Kim, S.-J.; Ahn, S.-M.; Kim, H.-W.; Choi, K.-S.; Kwon, H.-J. Tracing the Evolutionary Pathways of Serogroup O78 Avian Pathogenic Escherichia coli. Antibiotics 2023, 12, 1714. https://doi.org/10.3390/antibiotics12121714
Ha E-J, Hong S-M, Kim S-J, Ahn S-M, Kim H-W, Choi K-S, Kwon H-J. Tracing the Evolutionary Pathways of Serogroup O78 Avian Pathogenic Escherichia coli. Antibiotics. 2023; 12(12):1714. https://doi.org/10.3390/antibiotics12121714
Chicago/Turabian StyleHa, Eun-Jin, Seung-Min Hong, Seung-Ji Kim, Sun-Min Ahn, Ho-Won Kim, Kang-Seuk Choi, and Hyuk-Joon Kwon. 2023. "Tracing the Evolutionary Pathways of Serogroup O78 Avian Pathogenic Escherichia coli" Antibiotics 12, no. 12: 1714. https://doi.org/10.3390/antibiotics12121714