The Role of Salmonella Genomic Island 4 in Metal Tolerance of Salmonella enterica Serovar I 4,[5],12:i:- Pork Outbreak Isolate USDA15WA-1
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains, Mutant Construction, and Primers
2.2. Conjugation Studies
2.3. DNA Sequencing and Assembly
2.4. Phenotypic Microarrays
2.5. Transcriptional Analysis of USDA15WA-1 in Response to Copper Exposure
2.6. Swine Study
2.7. Microbiota Analyses
3. Results and Discussion
3.1. Salmonella Genomic Island 4 Transferred by Conjugation from Strain USDA15WA-1 to Serovar Typhimurium
3.2. The Presence of SGI-4 in Strain USDA15WA-1 Enhanced Tolerance to Multiple Metals
3.3. Copper Induced Gene Expression of Metal Tolerance Genes on Genomic Islands
3.4. In-Feed Supplementation with Elevated Concentrations of Zn and Cu as an Antimicrobial Slowed the Decline of Salmonella I 4,[5],12:i:- Fecal Shedding in Pigs
3.5. Alterations in the Porcine Microbiota in Response to In-Feed Zn/Cu Treatment
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
Appendix B
References
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Strain No. | Strain Background | Genotype | Phenotype * | Source |
---|---|---|---|---|
BSX 137 | USDA15WA-1, FSIS1503788, SX 238 | serovar I 4,[5],12:i:- | ASSuT | Glenn Tillman FSIS [6] |
SX 240 | USDA15WA-1, FSIS1503788 | serovar I 4,[5],12:i:- | ASSuT | Swine passaged [17] |
BSX 120 | UK-1, SB 26 | serovar Typhimurium | Nal | [18] |
BBS 1268 | USDA15WA-1 | pKD46-Gm | ASSuTGm, 30 °C | BSX 137/pKD46-GM; plasmid source [16] |
BBS 1270 | USDA15WA-1 | ΔSGI-4: neo | ASSuTKn | BBS 1268/oBBI 528/529-neo |
BBS 1356 | USDA15WA-1 | SGI-4Ωneo | ASSuTKn | BBS 1268/oBBI 542/543-neo |
BBS 1358 | UK-1 | SGI-4Ωneo | NalKn | BSX 120 x BBS 1356 |
BBS 1359 | UK-1 | SGI-4Ωneo | NalKn | BSX 120 x BBS 1356 |
BBS 1406 | UK-1 | SGI-4Ωneo | NalKn | BBS 1358small |
BBS 1407 | UK-1 | SGI-4Ωneo | NalKn | BBS 1358large |
Gene ID | Gene Name | 30 Min | 60 Min | Description | Location | ||
---|---|---|---|---|---|---|---|
Log2FC | FDR | Log2FC | FDR | ||||
AOL22_00855 | cueO | 4.3 | 5.02 × 10−34 | 4.2 | 7.55 × 10−31 | multicopper oxidase CueO | Core |
AOL22_02225 | mdsC | 3 | 7.80 × 10−9 | 1.7 | 1.85 × 10−9 | multidrug efflux transporter outer membrane subunit MdsC (GesC) | Core |
AOL22_02230 | mdsB | 3.5 | 5.39 × 10−8 | 2.8 | 2.35× 10−11 | multidrug efflux RND transporter permease subunit MdsB (GesB) | Core |
AOL22_02235 | mdsA | 5.3 | 6.59 × 10−12 | 4.8 | 6.80 × 10−16 | multidrug efflux RND transporter periplasmic adaptor subunit MdsA (GesA) | Core |
AOL22_02240 | golT | 7 | 2.09 × 10−28 | 6.3 | 1.33 × 10−18 | gold/copper-translocating P-type ATPase GolT | Core |
AOL22_02245 | golS | 5.9 | 3.38 × 10−29 | 5 | 2.55 × 10−27 | Au(I) sensor transcriptional regulator GolS | Core |
AOL22_02250 | golB | 6.9 | 1.35 × 10−97 | 6.5 | 2.12 × 10−102 | gold resistance metallochaperone GolB | Core |
AOL22_02995 | copA | 5.7 | 2.64 × 10−25 | 5.2 | 4.89 × 10−48 | copper-exporting P-type ATPase CopA | Core |
AOL22_05910 | scsA | 2.4 | 9.70 × 10−6 | 4.1 | 1.13 × 10−22 | copper resistance protein | Core |
AOL22_05915 | scsB | 6.2 | 7.68 × 10−37 | 7.8 | 2.48 × 10−88 | protein disulfide reductase | Core |
AOL22_05920 | scsC | 5.4 | 4.80 × 10−29 | 6.7 | 1.42 × 10−75 | disulfide bond formation protein DsbA | Core |
AOL22_05925 | scsD | 4.8 | 4.60 × 10−18 | 6.4 | 2.60 × 10−58 | protein disulfide oxidoreductase | Core |
AOL22_14670 | merE | 1.8 | 2.10 × 10−3 | 1.3 | 6.18 × 10−3 | broad-spectrum mercury transporter MerE | MDR |
AOL22_14675 | merD | 1.4 | 7.46 × 10−3 | 1.5 | 1.72 × 10−3 | mercury resistance co-regulator MerD | MDR |
AOL22_14680 | merA | 1.3 | 1.40 × 10−2 | 1.1 | 1.09 × 10−2 | mercury(II) reductase | MDR |
AOL22_14685 | merC | 1.4 | 4.45 × 10−3 | 1.2 | 4.41 × 10−3 | organomercurial transporter MerC | MDR |
AOL22_14690 | merP | 1.4 | 3.21 × 10−3 | 1.1 | 5.62 × 10−3 | mercury resistance system periplasmic binding protein MerP | MDR |
AOL22_14695 | merT | 1.6 | 1.49 × 10−3 | 1.5 | 1.00 × 10−3 | mercuric ion transporter MerT | MDR |
AOL22_23325 | arsR | 2.6 | 1.35 × 10−3 | 2 | 1.65 × 10−3 | transcriptional regulator | SGI-4 |
AOL22_23330 | arsD | 4.8 | 1.34 × 10−9 | 4 | 4.09 × 10−7 | arsenite efflux transporter metallochaperone ArsD | SGI-4 |
AOL22_23335 | arsA | 4.6 | 4.25 × 10−9 | 3.7 | 1.39 × 10−6 | arsenite efflux transporter ATPase subunit ArsA | SGI-4 |
AOL22_23340 | arsB | 4.5 | 9.60 × 10−8 | 3.9 | 1.56 × 10−6 | arsenic transporter | SGI-4 |
AOL22_23345 | arsC | 3.7 | 2.37 × 10−10 | 3 | 1.23 × 10−6 | arsenate reductase (glutaredoxin) | SGI-4 |
AOL22_23510 | silE | 9 | 2.29 × 10−53 | 7.5 | 1.55 × 10−32 | silver-binding protein SilE | SGI-4 |
AOL22_23515 | silS | 2.7 | 4.93 × 10−10 | 2 | 1.42 × 10−6 | copper/silver sensor histidine kinase SilS | SGI-4 |
AOL22_23520 | silR | 3.2 | 6.17 × 10−8 | 2.4 | 2.57 × 10−6 | copper/silver response regulator transcription factor SilR | SGI-4 |
AOL22_23525 | silC | 7 | 1.04 × 10−19 | 6.5 | 6.81 × 10−19 | Cu(+)/Ag(+) efflux RND transporter outer membrane channel SilC | SGI-4 |
AOL22_23530 | silF | 7.3 | 4.31 × 10−32 | 6.9 | 4.25 × 10−23 | copper ABC transporter substrate-binding protein | SGI-4 |
AOL22_23535 | silB | 7.5 | 3.63 × 10−25 | 7 | 2.39 × 10−21 | Cu(+)/Ag(+) efflux RND transporter periplasmic adaptor subunit SilB | SGI-4 |
AOL22_23540 | silA | 6.7 | 8.15 × 10−26 | 5.8 | 1.80 × 10−19 | Cu(+)/Ag(+) efflux RND transporter permease subunit SilA | SGI-4 |
AOL22_23545 | orf105 | 6.9 | 8.38 × 10−204 | 4.8 | 1.30 × 10−64 | hypothetical protein | SGI-4 |
AOL22_23550 | silP | 5.7 | 1.94 × 10−47 | 3.5 | 1.66 × 10−15 | Ag(+)-translocating P-type ATPase SilP | SGI-4 |
AOL22_23565 | pcoG | 2.3 | 6.85 × 10−8 | 0.71 | 5.20 × 10−2 | copper resistance protein | SGI-4 |
AOL22_23570 | pcoA | 2.4 | 9.92 × 10−19 | 2.3 | 1.10 × 10−25 | multicopper oxidase PcoA | SGI-4 |
AOL22_23575 | pcoB | 2.4 | 5.26 × 10−16 | 2.3 | 2.71 × 10−17 | copper resistance outer membrane transporter PcoB | SGI-4 |
AOL22_23580 | pcoC | 2.5 | 4.30 × 10−15 | 2.1 | 2.41 × 10−20 | copper resistance system metallochaperone PcoC | SGI-4 |
AOL22_23585 | pcoD | 1.7 | 4.43 × 10−7 | 1.4 | 4.73 × 10−6 | copper resistance inner membrane protein PcoD | SGI-4 |
AOL22_23590 | pcoR | 0.4 | 2.43 × 10−1 | 0.7 | 2.27 × 10−2 | copper response regulator transcription factor PcoR | SGI-4 |
AOL22_23595 | pcoS | 0.3 | 2.57 × 10−1 | 0.8 | 1.73 × 10−4 | copper resistance membrane spanning protein PcoS | SGI-4 |
AOL22_23600 | pcoE | 7.7 | 6.64 × 10−25 | 6.7 | 1.68 × 10−21 | copper-binding protein | SGI-4 |
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Bearson, B.L.; Trachsel, J.M.; Shippy, D.C.; Sivasankaran, S.K.; Kerr, B.J.; Loving, C.L.; Brunelle, B.W.; Curry, S.M.; Gabler, N.K.; Bearson, S.M.D. The Role of Salmonella Genomic Island 4 in Metal Tolerance of Salmonella enterica Serovar I 4,[5],12:i:- Pork Outbreak Isolate USDA15WA-1. Genes 2020, 11, 1291. https://0-doi-org.brum.beds.ac.uk/10.3390/genes11111291
Bearson BL, Trachsel JM, Shippy DC, Sivasankaran SK, Kerr BJ, Loving CL, Brunelle BW, Curry SM, Gabler NK, Bearson SMD. The Role of Salmonella Genomic Island 4 in Metal Tolerance of Salmonella enterica Serovar I 4,[5],12:i:- Pork Outbreak Isolate USDA15WA-1. Genes. 2020; 11(11):1291. https://0-doi-org.brum.beds.ac.uk/10.3390/genes11111291
Chicago/Turabian StyleBearson, Bradley L., Julian M. Trachsel, Daniel C. Shippy, Sathesh K. Sivasankaran, Brian J. Kerr, Crystal L. Loving, Brian W. Brunelle, Shelby M. Curry, Nicholas K. Gabler, and Shawn M. D. Bearson. 2020. "The Role of Salmonella Genomic Island 4 in Metal Tolerance of Salmonella enterica Serovar I 4,[5],12:i:- Pork Outbreak Isolate USDA15WA-1" Genes 11, no. 11: 1291. https://0-doi-org.brum.beds.ac.uk/10.3390/genes11111291