Roles of Aerotolerance, Biofilm Formation, and Viable but Non-Culturable State in the Survival of Campylobacter jejuni in Poultry Processing Environments
Abstract
1. Introduction
2. Physiology of Campylobacter
3. Incidence of Campylobacter in Poultry Processing Facilities
4. Stress Encountered by Campylobacter inside Poultry Processing Facilities
4.1. Aerobic Stress
4.2. Heat Stress
4.3. Refrigeration and Freezing Stress
4.4. Osmotic Stress
4.5. UV Stress
4.6. Acid Stress
5. Potential Survival Mechanisms
5.1. Aerotolerance Development
5.2. Biofilm Formation
Genes Involved in Biofilm Formation by Campylobacter
5.3. Viable but non Culturable (VBNC) State Formation
6. Future Research to Fill Current Knowledge Gaps
7. Conclusions
Source of Contamination | Country of Occurrence | Incidence of C. jejuni | References |
---|---|---|---|
Birds with feathers, birds at rehang, birds after evisceration, immediately after entering chiller, after exiting chlorinated chill tank | USA—Georgia | 87.27%, (n = 55) | [123] |
Rehang and post chill whole carcass rinse | USA—Alabama, Arkansas, California, Delaware, Georgia, Indiana, Missouri, North Carolina, South Carolina, Tennessee, Texas, Virginia, and West Virginia | Rehang—74.5%, (n = 800) Post-chill—34.90%, (n = 800) | [124] |
Feces, pasture soil, whole carcass rinse directly after processing (WCR-P), final product whole carcass rinse after chilling and storage time (WCR-F), and ceca samples collected during processing from each farm | Southeastern USA from March 2014 to November 2017 | 39.08%, (n = 2305) | [125] |
Air, feces-litter, feed pans and water lines | USA—Virginia | 26.66%, (n = 120) | [126] |
Fecal and environmental samples | USA—North Carolina | Fecal: 29.50%; (n = 400) Environmental sample: 1%, (n = 500) | [127] |
Pre-scald (feather and skin) | USA—Delmarva Peninsula | 77%, (n = 48) | [128] |
Evisceration | USA | 96–100%, (n = 48) | [129] |
Slaughterhouse | Brazil- Parana, santa Catarina and Rio Grande do Sul | Campylobacter spp.—35.84% (n = 816) C. jejuni—78.47% (n = 144) | [130] |
Defeathering, Evisceration, Shackles, Converyor belt | North of Spain | Defeathering—80% (n = 30) Eviseration—100% (n = 39) Shackles—100% (n = 23) Converyor belt—96.6% (n = 29) | [131] |
Defeathering machine, evisceration machine, conveyor belts, scald tank, water | France | 87% (34/39) | [45] |
Stressors | Gene Involved | Gene Function | References |
---|---|---|---|
Heat stress |
| Express DnaJ chaperone protein-protein folding and heat shock response | [51] |
| Component of RacR-RacS temperature-responsive signal transduction system | [53] | |
| High temperature requirement A (HtrA)-like protease and chaperones | [91] | |
| Express iron sequestration ferritin protein (Dps) | [132] | |
| Express DnaK chaperonin- protein folding | ||
Refrigeration and freezing stress |
| Superoxide dismutase | [59] |
| S-ribosylhomocysteinase-catalyzes the formation of autoinducer-2 (AI-2) molecules and homocysteine | [133] | |
Osmotic stress |
| Capsule export gene-encodes capsule export apparatus | [65] |
Acid stress |
| ATP-dependent Protease-heat shock gene | [79] |
| Thioredoxin-disulfide reductase-protein folding | [87] | |
| Ferric uptake regulator gene | [88] | |
UV stress | recA | Express recA protein involved in DNA repair | [78] |
Gene | Gene Product or Function | Involved Function in Aerotolerance | References |
---|---|---|---|
ahpC | Alkyl hydroperoxide reductase-Antioxidant | Antioxidant | [40,90] |
katA | Catalase | Peroxide detoxification | [90] |
sodB | Iron co-factored superoxide dismutase- | Antioxidant | [90] |
fdxA | Ferredoxin A-cyclophilin gene | Antioxidant | [93] |
htrA | High temperature requirement-A protease | Removal of misfolded proteins as a result of oxygen stress | [92] |
tpx | Thiol peroxidase- | Scavenges molecular oxygen | [96] |
bcpb | Express Bacterioferritin comigratory protein | Regulate oxidative stress by attacking molecular oxygen | [96] |
ctb | Truncated hemoglobin | Oxygen-protective physiological role by increasing oxygen uptake rates | [94] |
Cj1556 | MarR family transcriptional regulator | Oxidative stress response | [95] |
Gene | Gene Product or Function | Involved Function in Biofilm | References |
---|---|---|---|
flaA | Glycosylated structural flagellins-A | Involved in cell associated with motility | [106] |
luxS | S-ribosylhomocysteianse | Quorum sensing | [17] |
cadF | Campylobacter adhesion to fibronectin | Adhesion | [17] |
dnaJ | Chaperone DnaJ | Stress response | [107] |
cbrA | Campylobacter bile resistance regulator | Stress response | [107] |
htrA | High temperature requirement A | Stress response | [107] |
sodB | Superoxide dismutase | Stress response | [107] |
ahpC | Alkyl hydroperoxide reductase | Involved in oxidative stress response | [107] |
peb4 | encode homolog of cluster 3 binding protein | adhesion | [109] |
trxA | Thioredoxin A | Involved in oxidative stress response | [18] |
trxB | Thioredoxin B | Involved in oxidative stress response | [18] |
ilvE | Branched chain amino transferases for leucine, isoleucine, and valine | Involved in oxidative stress response | [18] |
nuoC | NuoC- subunit of complex I (ubiquinone oxidoreductase) | Assembly or the stability of ubiquinone oxidoreductase | [18] |
Gene | Gene Product or Function | Involved Function in VBNC | References |
---|---|---|---|
ppk1 | Poly phosphate kinase 1-codes for PPK1 enzyme mediates the synthesis of poly P | Mutant of ppk1 decreased the accumulation of poly P-decreased stress response | [134] |
cadF | Code 37 kDa adhesin-bind to fibronectin and mediates bacteria-host interaction | Retain ability to adhere to host cells | [116] |
flaA, flab | Flagellin-Involved bacteria internalization | Decreased expression- conserve energy for metabolism | [29] |
cdtA, cdtB and cdtC | Cytolethal distending toxins-arrest G2/M phase of cell cycle causing cell death | Decreased expression-conserve energy for metabolism | [29] |
ciaB | Campylobacter invasion antigen B | Decreased expression-conserve energy for metabolism | [29] |
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Pokhrel, D.; Thames, H.T.; Zhang, L.; Dinh, T.T.N.; Schilling, W.; White, S.B.; Ramachandran, R.; Theradiyil Sukumaran, A. Roles of Aerotolerance, Biofilm Formation, and Viable but Non-Culturable State in the Survival of Campylobacter jejuni in Poultry Processing Environments. Microorganisms 2022, 10, 2165. https://doi.org/10.3390/microorganisms10112165
Pokhrel D, Thames HT, Zhang L, Dinh TTN, Schilling W, White SB, Ramachandran R, Theradiyil Sukumaran A. Roles of Aerotolerance, Biofilm Formation, and Viable but Non-Culturable State in the Survival of Campylobacter jejuni in Poultry Processing Environments. Microorganisms. 2022; 10(11):2165. https://doi.org/10.3390/microorganisms10112165
Chicago/Turabian StylePokhrel, Diksha, Hudson T. Thames, Li Zhang, Thu T. N. Dinh, Wes Schilling, Shecoya B. White, Reshma Ramachandran, and Anuraj Theradiyil Sukumaran. 2022. "Roles of Aerotolerance, Biofilm Formation, and Viable but Non-Culturable State in the Survival of Campylobacter jejuni in Poultry Processing Environments" Microorganisms 10, no. 11: 2165. https://doi.org/10.3390/microorganisms10112165
APA StylePokhrel, D., Thames, H. T., Zhang, L., Dinh, T. T. N., Schilling, W., White, S. B., Ramachandran, R., & Theradiyil Sukumaran, A. (2022). Roles of Aerotolerance, Biofilm Formation, and Viable but Non-Culturable State in the Survival of Campylobacter jejuni in Poultry Processing Environments. Microorganisms, 10(11), 2165. https://doi.org/10.3390/microorganisms10112165