Fitness of Outbreak and Environmental Strains of Escherichia coli O157:H7 in Aerosolizable Soil and Association of Clonal Variation in Stress Gene Regulation
Abstract
:1. Introduction
2. Results and Discussion
2.1. Survival of EcO157 Strains in Moist Soil
2.2. Fitness of EcO157 Strains in Soil Initially Adjusted to 50% WHC
Strains a | Origin | MLVA Type | Curli Proportion, % | D-value | Source |
---|---|---|---|---|---|
RM6331 | Human | 163 | 0 | 7.5 | 2006, Oregon State Public Health Lab, spinach outbreak, OR |
RM6653 | Human | 163 | 80 | 7.1 | 2006, CDC, spinach outbreak, WI |
RM6654 | Human | 163 | 50 | 6.1 | 2006, CDC, spinach outbreak, NM |
RM6657 | Human | 163 | 70 | 6.1 | 2006, CDC, spinach outbreak, UT |
RM6663 | Human | 163 | 30 | 6.4 | 2006, CDC, spinach outbreak, PA |
RM6069 | Human | 163 | 100 | 1.4 | 2006 spinach outbreak, PA [36] |
RM11780 | Human | 964 | 0 | 7.4 | 2010, Oahu, Korean Barbecue, HI |
RM11784 | Human | 965 | 0 | 10.8 | 2010, Oahu, Korean Barbecue, HI |
RM6067 | Spinach | 163 | 50 | 10.3 | 2006 spinach outbreak, PA [36] |
RM6155 | Pig feces | 163 | 0 | 12.3 | 2006, Ranch A pasture, CA |
RM6101 | Pig feces | 176 | 0 | 10 | 2006 spinach outbreak, CA [36] |
RM6102 | Water | 176 | 0 | 8.9 | 2006 spinach outbreak, CA [36] |
RM9854 | Soil | 792 | 0 | 9.5 | 2009, Ranch J, CSREES b study, CA |
RM9834 | Soil | 778 | 0 | 10.8 | 2009, Ranch J, CSREES study, CA |
RM9853 | Soil | 778 | NTc | 8.4 | 2009, Ranch J, CSREES study, CA |
RM6149 | Soil | 176 | NT | 11.7 | 2006, Ranch A pasture soil/dust, CA |
RM1484 | Apple juice | 23 | 100 | 6 | 1996, FDA, apple juice outbreak, CA |
RM6103 | Cow feces | 163 | 0 | 8.3 | 2006 spinach outbreak, CA [36] |
RM6107 | Cow feces | 176 | 0 | 10.8 | 2006, Ranch A pasture, CA |
RM6436 | Cow feces | 173 | 0 | 1.9 | 2006 spinach outbreak, CA [36] |
RM5038 | Cow feces | 15 | NT | 9 | 2005, Salinas, CA |
RM10910 | Cow feces | 881 | NT | 8.5 | 2009, CSREES study, CA |
RM6704 | Cow feces | 346 | NT | 4.7 | 2007, Sierra Foothills, Browns valley, CA |
RM7024 | Cow feces | 416 | NT | 6.8 | 2007, Sierra Foothills, Browns valley, CA |
RM6121 | Cow feces | 187 | NT | 11.5 | 2006, Ranch J, replacement heifers, CA |
RM7354 | Cow feces | 186 | NT | 9.5 | 2007 Leafy green outbreak (suspected), HI |
RM7469 | Cow feces | 534 | NT | 6.1 | 2008, CSREES study, CA |
RM9562 | Cow feces | 769 | NT | 5.2 | 2009, CSREES study, CA |
RM6666 | Cow feces | 352 | NT | 6.2 | 2007, Sonoma dairy, CA |
RM7437 | Cow feces | 489 | NT | 7.5 | 2008, CSREES study, CA |
RM8436 | Cow feces | 490 | NT | 6.2 | 2008, CSREES study, CA |
RM7438 | Cow feces | 486 | NT | 5.1 | 2008, CSREES study, CA |
RM6009 | Moore swab | 158 | NT | 5.6 | 2006 spinach outbreak, CA [36] |
RM5686 | Moore swab | 89 | NT | 5.7 | 2006 spinach outbreak, CA [36] |
RM5724 | Moore swab | 143 | NT | 4.3 | 2006 spinach outbreak, CA [36] |
2.3. Survival of Curli Variants in Soil
Strain | Origin | MLVA Type a | D-value, d b | ||||
---|---|---|---|---|---|---|---|
Parent | C+ | C− | Parent c | C+ | C− | ||
RM1484 | Apple juice | 23 | 23 | 23 | 6.0 ± 0.3 | 5.4 ± 1.4 | 10.1 ± 2.9 |
RM6069 | Human | 163 | 163 | 361 | 1.4 ± 0.0 | 1.4 ± 0.0 | 6.1 ± 2.0 |
RM6067 | Spinach | 163 | 975 | 164 | 10.3 ± 2.5 | 1.4 ± 0.0 | 20.2 ± 11.0 |
RM6103 | Cow feces | 163 | 163 | 163 | 12.5 ± 1.3 | 4.8 ± 1.2 | 19.9 ± 10.8 |
2.4. Survival of EcO157 in Soil after Three Successive Transfers in Soil
Strain a | Origin | State | D-values b | C+ variants, % | ||
---|---|---|---|---|---|---|
5 d | 18 d | Parent c | Post Exposure | |||
RM6069 | Human | PA | 7.0 | 2.6 | 100 | 90 |
RM6653 | Human | WI | 7.1 | 4.5 | 80 | 50 |
RM6654 | Human | NM | 6.1 | 7.6 | 50 | 10 |
RM6663 | Human | PA | 6.4 | 8.2 | 30 | 0 |
RM6331 | Human | OR | 7.5 | 7.6 | 0 | 0 |
RM6155 | Pig feces | CA | 7.9 | 8.4 | 0 | 0 |
RM6103 | Cow feces | CA | 9.8 | 7.1 | 0 | 0 |
RM6067 | Spinach | CA | 6.0 | 8.2 | 50 | 0 |
RM9834 | Soil | CA | 8.9 | 7.3 | 0 | 0 |
2.5. Expression of Selective Stress Genes of Curli Variants that Survived Three Passes in Soil
2.6. Clonal Variation in rpoS Gene Sequence of EcO157 Strains
2.7. Discussion
3. Materials and Methods
3.1. Soil used in EcO157 Fitness Studies
3.2. Strains of EcO157
3.3. Preparation and Enumeration of Strains for Inoculation of Soil
3.4. Fitness of EcO157 Strains in Soil from a Produce Field
3.5. Fitness of Phenotypically Variant Subpopulations
3.6. MLVA Genotyping of C+ and C− Variant Clones of EcO157 Strains
3.7. Measurement of Surviving EcO157 Phenotypes during and after Successive Transfers in Soil
3.8. Gene Expression by Clones Surviving Soil Exposure
3.9. Sequencing of RpoS from Clones of EcO157 Surviving Soil Exposure
3.10. Statistical Methods
4. Conclusions
Acknowledgments
Author Contributions
Supplementary Information
Stress Gene | Percent Clones Downregulated (Range of Fold Change a) | |||
---|---|---|---|---|
RM6653 | RM6069 | RM6067 | RM9834 | |
rpoS | 0 (6–83) | 100 (−7–−1) | 80 (−4–3) | 60 (−4–3) |
slp | 40 (−3–5) | 100 (−4–−1) | 80 (−2–1) | 100 (−2–−1) |
osmY | 60 (−13–2) | 100 (−56–−2) | 100 (−7–−1) | 70 (−2–2) |
katP | 90 (−5–1) | 100 (−2–1) | 100 (−3–−2) | 80 (−2–1) |
hdeA | 20 (−1–5) | 90 (−4–1) | 90 (−3–1) | 60 (−2–1) |
oxyS | 30 (−2–2) | 30 (−2–27) | 70 (−2–1) | 100 (−3–−1) |
marA | 30 (−1–2) | 60 (−2–1) | 70 (−2–2) | 80 (−2–1) |
marR | 30 (−2–2) | 50 (−1–1) | 90 (−2–1) | 100 (−29–−1) |
nemR | 20 (−1–4) | 80 (−2–2) | 100 (−2–−1) | 70 (−2–1) |
soxS | 20 (−1–3) | 40 (−2–2) | 60 (−2–2) | 100 (−2–−1) |
ahpF | 70 (−3–2) | 60 (−2–1) | 90 (−2–1) | 30 (−1–2) |
gloA | 20 (−2–2) | 60 (−3–1) | 90 (−3–−1) | 80 (−2–1) |
Gene | Gene Product/Function | Forward/Reverse Primers, 5'→3' (reference) |
---|---|---|
ahpF | Alkyl hydroperoxide reductase, subunit F | GCAGATTCGCCATATTGACG GCCCTGACCAAACTCTTTCC [31] |
gloA | Glyoxalase I | ACTCACTGGCGTTTGTTGG GACCGGCGTCTTTCTCTTC [31] |
gyrB | DNA gyrase, subunit B | GCAAGCCACGCAGTTTCTC GGAAGCCGACCTCTCTGATG [31] |
hdeA | Acid resistance protein | GCTTCTTCTGCCAGTTGTGAGCAA AGCCAGGAAATCTTCACAGGTCCA [31] |
katP | EHEC catalase/peroxidase | CGGGAAACTTCAGAAACCTC GCCACAGTCTCCTCATCATC [31] |
marA | Multiple antibiotic resistance | CGAGGACAACCTGGAATCAC TGCGGCGGAACATCAAAG [31] |
marR | Multiple antibiotic resistance | CGCGGCGTGTATTACTCC GGTTCGGCAACCTTTCTACC [31] |
nemR | Predicted DNA-binding transcriptional regulator | CCATTACGCCACATATCACC TATCACGGCCATTTTCCAG [31] |
osmY | Hyperosmotically inducible periplasmic protein | ACGTTGCGACGCTAAAGAA CATGACGGGAAGGGACGT [32] |
oxyS | Oxidative stress regulator | GAGCGGCACCTCTTTTAACCCTTG CCTGGAGATCCGCAAAAGTTCACG [31] |
rpoS | RNA polymerase, sigma S (sigma 38) factor | CGCCGGATGATCGAGAGTAA GAGGCCAATTTCACGACCTA [50] |
slp | Outer membrane lipoprotein, starvation lipoprotein | AACCTGTGGGATTACGGCTATGGT AGGTGTTACCTGACTCACCGCATT [32] |
soxS | Global transcription regulator for superoxide response | GTCGTCGCAAAAAAATCAGG TGGGAGTGCGATCAAACTG [31] |
Method S1. Sequencing of rpoS gene from clones of EcO157 strains surviving soil exposure
Conflicts of Interest
References
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Ravva, S.V.; Cooley, M.B.; Sarreal, C.Z.; Mandrell, R.E. Fitness of Outbreak and Environmental Strains of Escherichia coli O157:H7 in Aerosolizable Soil and Association of Clonal Variation in Stress Gene Regulation. Pathogens 2014, 3, 528-548. https://doi.org/10.3390/pathogens3030528
Ravva SV, Cooley MB, Sarreal CZ, Mandrell RE. Fitness of Outbreak and Environmental Strains of Escherichia coli O157:H7 in Aerosolizable Soil and Association of Clonal Variation in Stress Gene Regulation. Pathogens. 2014; 3(3):528-548. https://doi.org/10.3390/pathogens3030528
Chicago/Turabian StyleRavva, Subbarao V., Michael B. Cooley, Chester Z. Sarreal, and Robert E. Mandrell. 2014. "Fitness of Outbreak and Environmental Strains of Escherichia coli O157:H7 in Aerosolizable Soil and Association of Clonal Variation in Stress Gene Regulation" Pathogens 3, no. 3: 528-548. https://doi.org/10.3390/pathogens3030528
APA StyleRavva, S. V., Cooley, M. B., Sarreal, C. Z., & Mandrell, R. E. (2014). Fitness of Outbreak and Environmental Strains of Escherichia coli O157:H7 in Aerosolizable Soil and Association of Clonal Variation in Stress Gene Regulation. Pathogens, 3(3), 528-548. https://doi.org/10.3390/pathogens3030528