Location: Food and Feed Safety Research
2023 Annual Report
Objectives
Objective 1: Characterize the immune-metabolic signatures of the host:pathogen interactome following Salmonella and Campylobacter infection in the cecum that transforms host defenses from 'disease resistance' to 'disease tolerance' and mitigates long-term persistent intestinal infection in broilers chickens.
Objective 2: Determine the intestinal kinome profile and antimicrobial resistance patterns associated with Salmonella and Campylobacter colonization in broiler chickens with high or low concentrations of these foodborne pathogens.
Objective 3: Develop new strategies (including immunologic training) to reduce foodborne pathogens by targeting neonatal poultry gut health via stimulating the development and maturation of the intestinal immune system.
Sub-objective 3.A: Deliver non-nutritional dietary feed additives to breeder chickens (hens and roosters) to induce /enhance trans-generational trained innate immunity as both a prophylactic and as a therapeutic agent in neonatal chickens against foodborne pathogens.
Sub-objective 3.B: Evaluate a novel innate immune therapeutic as an alternative to antibiotics that targets innate immunity based on the ability of the immune system to detect bacterial viability through the recognition of viability-associated microbial associated molecular patterns (vita-MAMPs).
Sub-objective 3.C: Develop a novel immunogenic probiotic to improve neonatal poultry gut health and stimulate the development and maturation of the intestinal immune system.
Objective 4: Develop intervention strategies and alternatives to antibiotics to reduce the bacterial load of foodborne pathogens during pre-harvest poultry production.
Objective 5: Investigate the interaction between yeast and fungi and foodborne bacteria to determine their role as commensals, inhibitors, or their use as alternatives to antibiotics as pre-and probiotics.
Approach
Despite control efforts, foodborne illnesses due to Salmonella continues to impact the consumer. Poultry are commonly identified as a major source of Salmonella. We will take a multi-faceted approach to develop urgently needed new control strategies against Salmonella, and our integrated approaches will identify and evaluate applied and basic pre-harvest approaches to reduce Salmonella in poultry. Based on previous research and collaborations with industry, we will identify and/or modify management practices to reduce foodborne pathogen load and will address environmental conditions associated with higher risks that enable pathogen survival and growth. Direct and indirect modulation of gut microbiome-innate immune interactome will be evaluated to determine which natural host mechanisms can be exploited to strengthen therapeutic benefit. Modulating the innate immune response has considerable potential to induce a profound and rapid cross-protection against multiple serovars of foodborne pathogens. Salmonella have evolved a unique survival strategy in poultry that minimizes host defenses during the initial infection and then exploits and/or induces a dramatic immunometabolic reprogramming in the cecum that alters the host defense to induce a disease tolerance. Therefore, a component of the research will concentrate on modulatory mechanisms (vaccination, pro- and postbiotic) to counter these reprogramming mechanisms and lead to the development of novel immunometabolic therapeutic strategies. This research will enhance the microbiological safety of poultry and reduce potential antimicrobial resistance in animal agriculture and public health.
Progress Report
Work in FY 2023 under Objectives 1 and 2 identified crucial elements of the intestinal mucosal immune system that enhance the ability of poultry to fight off pathogenic microbes while maintaining a state of tolerance to the diverse and beneficial intestinal microbes. The chicken metabolome (the totality of biochemical metabolites within an organism) was profiled, and bioinformatics data is being tabulated and evaluated. In research under Objective 3, chicks were hatched from breeder hens on a control diet, or on a diet supplemented with an immune-boosting antibiotic alternative. The chicks from hens fed the dietary supplement were more resistant to Salmonella colonization, showing they had an enhanced immune response and thus a level of transgenerational protection passed on from the breeder hens. Immunological evaluations showed the supplemented chicks to have increased innate immune parameters at the gut level that likely contributed to the reduced Salmonella colonization and enhanced bacterial clearance. Additional research under Objective 3 evaluated a novel innate immune therapeutic, as an alternative to antibiotics, by targeting innate immunity based on the ability of the immune system to detect bacterial viability through the recognition of viability-associated microbial associated molecular patterns. In other Objective 3 research, work demonstrated for the first time that segmented filamentous bacteria (SFB) spore containing inoculum reduces gut permeability in young chickens and stimulates innate and adaptive immune responses. Additionally, SFB-based treatment can potentially-protect chickens from enteric pathogens, partly due to its unique ability to trigger a protective T cell mediated immune response. Under Objective 4, routes by which Salmonella infect turkeys were identified; the findings have significant food safety implications in commercial turkey production. This work is of high interest to the industry given its promise in developing pre-harvest intervention strategies that can be incorporated into commercial turkey production to enhance microbial food safety.
Accomplishments
1. Infection routes of Salmonella in turkeys. Growing turkeys are susceptible to colonization by Salmonella types (serovars) that can cause food poisoning in humans if the meat products are contaminated during processing. The turkey industry is in critical need of effective strategies to ensure that turkey food products reaching the consumer are microbiologically safe. ARS researchers at College Station, Texas, working closely with key turkey industry scientists and managers, established that Salmonella can be recovered at different anatomical locations in turkeys including the blood, joints, and other systemic locations. This accomplishment is important because knowing that Salmonella can infect different areas of the body of growing turkeys is critical to the development of new technology and/or management strategies to ensure microbiological safety of turkey food products. The industry and relevant U.S. regulatory agencies are well aware of and highly supportive of this work.
2. Transgenerational protection of chicks against Salmonella. Foodborne pathogen reduction in animal agriculture requires a combination of intervention strategies to effectively reduce the number of foodborne illnesses. ARS researchers at College Station, Texas, established that chicks hatched from breeder hens on a diet supplemented with an immune-boosting antibiotic alternative were more resistant to Salmonella colonization than were chicks from non-supplemented hens. This clearly established that the chicks from supplemented breeder hens had an enhanced immune response and that a level of transgenerational protection had been passed to them by the mother hen. Immunological evaluations showed the chicks had increased innate immune parameters at the gut level that likely contributed to the reduced Salmonella colonization and enhanced bacterial clearance. This accomplishment is important because of the increased consumer demand for antibiotic-free products, increased risk of antibiotic resistant bacteria, and the need by the poultry industry to find suitable antibiotic alternatives that will promote bird health and performance. This is the first documentation that innate immunity can be induced in the breeder hen, transmitted to her progeny, and result in protection of her chicks against Salmonella infection during the first few days post-hatch.
3. Beneficial gut bacteria protect neonatal chicks. Salmonella is a known foodborne bacteria that infects/colonizes the intestinal tract of commercially grown poultry, and that ultimately can cause food poisoning in people if the bacteria contaminate meat products during processing. There is ongoing need for new technology that can be economically implemented by the poultry industry to minimize or prevent such infections. ARS researchers at College Station, Texas, discovered that a class of harmless microorganisms known as segmented filamentous bacteria (SFB), when administered orally to young chickens, are effective in preventing subsequent colonization by Salmonella. The apparent mode of action is that SFB binds intimately with the intestinal wall of the living chickens and thus "blocks" the space or binding sites that Salmonella or other harmful bacteria might otherwise occupy. This accomplishment is important because it represents discovery of a new approach to bird health and food safety that, if successfully implemented in commercial poultry production in a cost-effective manner, will significantly enhance the microbial safety of poultry meat products reaching the consumer.
Review Publications
Genovese, K.J., He, H., Swaggerty, C.L., Byrd II, J.A., Kogut, M.H. 2023. Leukocyte response to Campylobacter intra-abdominal infection in one day old leghorn chickens. Microorganisms. 11(3). Article 613. https://doi.org/10.3390/microorganisms11030613.
Johnson, C.N., Arsenault, R.J., Piva, A., Grilli, E., Swaggerty, C.L. 2023. A microencapsulated feed additive containing organic acids and botanicals has a distinct effect on proliferative and metabolic related signaling in the jejunum and ileum of broiler chickens. Frontiers in Physiology. 14. Article 1147483. https://doi.org/10.3389/fphys.2023.1147483.
Swaggerty, C.L., Malheiros, R.D., Lahaye, L., Byrd II, J.A., Genovese, K.J., He, L.H., Santin, E., Kogut, M.H. 2023. Addition of a protected complex of biofactors and antioxidants to breeder hen diets confers transgenerational protection against Salmonella enterica serovar Enteritidis in progeny chicks. Poultry Science. 102(4). Article 102531. https://doi.org/10.1016/j.psj.2023.102531.
Dittoe, D., Johnson, C.N., Byrd II, J.A., Ricke, S.C., Piva, A., Grilli, E., Swaggerty, C.L. 2023. Impact of a blend of microencapsulated organic acids and botanicals on the microbiome of commercial broiler breeders under clinical necrotic enteritis. Animals. 13(10). Article 1627. https://doi.org/10.3390/ani13101627.
He, L.H., Genovese, K.J., Arsenault, R.J., Johnson, C.N., Swaggerty, C.L., Byrd II, J.A., Kogut, M.H. 2023. M2 polarization and inhibition of host cell glycolysis contributes intracellular survival of Salmonella strains in chicken macrophage HD-11 cells. Microorganisms. 11(7). Article 1838. https://doi.org/10.3390/microorganisms11071838.
Dal Point, G.C., Lee, A., Bortoluzzi, C., Farnell, Y., Gougoulias, C., Kogut, M.H. 2022. Novel model for chronic intestinal inflammation in chickens: (2) immunologic mechanism behind the inflammatory response. Developmental and Comparative Immunology. 138. Article 104524. https://doi.org/10.1016/j.dci.2022.104524.
Kogut, M.H., Fernandez-Miyakawa, M. 2022. Editorial: Functional mechanisms at the avian gut microbiome-intestinal immunity interface and its regulation of avian physiological responses. Frontiers in Physiology. 13. Article 1063102. https://doi.org/10.3389/fphys.2022.1063102.
