The effects of a high-flavonoid corn cultivar on the gastrointestinal tract microbiota in chickens undergoing necrotic enteritis

Authors: BUIATTE, VINICIUS - Pennsylvania State University; Proszkowiec-Weglarz, Monika; Miska, Kate; DOMINGUEZ, DORIAN - Animal And Plant Health Inspection Service (APHIS); MAHMOUD, MAHMOUD - Pennsylvania State University; CHOPRA, SURINDER - Pennsylvania State University; LESKO, TYLER - Pennsylvania State University; Jenkins, Mark; LORENZONI, GINO ALBERTO - Pennsylvania State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/3/2024
Publication Date: 9/17/2024
Citation: Buiatte, V., Proszkowiec-Wegla, M.K., Miska, K.B., Dominguez, D., Mahmoud, M., Chopra, S., Lesko, T., Jenkins, M.C., Lorenzoni, G. 2024. The effects of a high-flavonoid corn cultivar on the gastrointestinal tract microbiota in chickens undergoing necrotic enteritis. PLOS ONE. 19((9). Article e0307333. https://doi.org/10.1371/journal.pone.0307333.
DOI: https://doi.org/10.1371/journal.pone.0307333

Interpretive Summary: Broiler type chickens are raised for meat production however their husbandry can be challenging due to several diseases which can affect the flocks causing decrease in weight gain and mortality, which results in economic losses to poultry producers. One of the diseases which can cause gastrointestinal symptoms in broilers, resulting in diarrhea, intestinal lesions, decreased interest in feed, and mortality is necrotic enteritis. This is an opportunistic infection caused by a bacterium (Clostridium perfringens), which occurs when intestinal health of the chickens in compromised by feed type, stress, parasitic infection, immune deficiency. Because many of the antibiotics which have been previously used to treat this disease are no longer available due to regulations, alternatives to antibiotics are being sought. In the current study, a strain of corn which is high in flavonoid compounds was fed to chicks with necrotic enteritis. Flavonoids are naturally occurring in plants, are anti-inflammatory, and have anti-microbial properties. In a previous study it was found that addition of high flavonoid corn decreased mortality by 50% and decreased intestinal lesions. In the current study we determined the changes in the microbiota of the small intestine (jejunum and ileum). Diversity of the microbiota (within and between populations) was observed in the ileum but not jejunum, possibly because more bacterial species are present in the ileum compared to the jejunum. The abundance of C. perfringens was lower in the infected birds which were fed with high flavonoid corn, suggesting that flavonoids in the corn may have a direct effect on decreasing the numbers of bacteria which cause necrotic enteritis. The abundance of Lactobacillus, which is thought to be beneficial bacteria that produces lactic acid also changed in response to the diets. In summary, the corn cultivar which is high in flavonoid compounds decreased the symptoms of necrotic enteritis, possibly by reducing the abundance of C. perfringens in the small intestine of broiler chickens. In the current study we investigated the changes in the microbiome of the ceca (large intestine) in chickens eating high flavonoid corn. We found that most of the microbiota changes were due to infection rather than diet. Infection affected the diversity of the bacteria present in the gut, and found that Escherichia coli, and Enterococcus cecorum, which are both opportunistic pathogens, were higher in birds with necrotic enteritis. Interestingly, the level of lactic acid bacteria which are thought to beneficial were also increased in infected chickens. Even though high flavonoid corn had a positive impact on mortality and intestinal health, it did not have many significant effects on the bacteria residing in the ceca, therefore the mechanism of action of flavonoid compounds in broiler chickens with necrotic enteritis must be further investigated.

Technical Abstract: The search for alternative therapies to antimicrobial growth promoters (AGP) in poultry production has gained momentum in the past years because of consumer preference and government restrictions on the use of AGP in animal production. Flavonoids are plant-derived metabolites that have been studied for their health-promoting properties that could potentially be used as an alternative to AGP in poultry. In a previous study, we showed that the inclusion of a flavonoid-rich corn cultivar (PennHFD1) in the diet improved the health of broilers undergoing necrotic enteritis. However, the mechanisms of action by which the PennHFD1-based diet ameliorated necrotic enteritis are unknown. This study describes the microbial diversity and composition of the jejunum and ileum of chickens co-infected with Eimeria maxima and Clostridium perfringens and treated with a high-flavonoid corn-based diet. Luminal content and mucosal samples from the jejunum and ileum were collected for DNA extraction, 16S rRNA amplicon sequencing and data analyses. The infection model and the dietary treatments significantly changed the alfa and beta diversities of the ileal samples (mucosa and luminal content), but not those of the jejunal samples. The microbial composition revealed that birds fed the high-flavonoid corn diet had a lower relative abundance of C. perfringens compared to birds fed the commercial corn diet. The treatments also changed the relative abundance of other bacteria that are related to gut health, such as Lactobacillus. We concluded that both the infection model and the dietary high-flavonoid corn changed the broilers’ gut microbial diversity and composition. In addition, the decrease in the relative abundance of C. perfringens was associated with a decrease in mortality and intestinal lesions due to necrotic enteritis. Collecting different segments and sample types provided a broader understanding of the changes in the gut microbiota among treatments.