Subclinical doses of dietary fumonisins and deoxynivalenol causes cecal microbiota dysbiosis in broiler chickens challenged with clostridium perfringens

Authors: Shanmugasundaram, Revathi; LOURENCO, JEFERSON - University Of Georgia; HAKEEM, WALID - University Of Georgia; DYCUS, MADISON - University Of Georgia; APPLEGATE, TODD - University Of Georgia

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/13/2023
Publication Date: 4/3/2023
Citation: Shanmugasundaram, R., Lourenco, J., Hakeem, W.A., Dycus, M., Applegate, T. 2023. Subclinical doses of dietary fumonisins and deoxynivalenol causes cecal microbiota dysbiosis in broiler chickens challenged with clostridium perfringens. Frontiers in Microbiology. 14:1-14. https://doi.org/10.3389/fmicb.2023.1106604.
DOI: https://doi.org/10.3389/fmicb.2023.1106604

Interpretive Summary: Microbes living in the gut of animals are considered key players in overall health and may play a pivotal role in the detoxification of orally ingested fungal toxins (mycotoxins) contaminating feed. Fusarium species such as F. verticillioides and F. graminearum produce multiple mycotoxins having negative impacts on chicken production, immunity, and health. However, no information is available on the impacts of chicken gut microbes on moderating the effects of combined mycotoxins fumonisins (FUM) and deoxynivalenol (DON). Neither is information available on the effects of mycotoxins on the gut microbes themselves. Hence, in this study, the gut bacterial compositions were assessed based on standard procedures. Our study demonstrated a direct relationship between gut microbes, mycotoxins, and host performance. Exposure to combined FUM and DON decreases the relative abundance of bacterial families involved in the biodegradation of FUM and DON. The decrease in the relative abundance of bacterial families induces dysbiosis in the microbiota, thereby causing subclinical necrotic enteritis. Continuous exposure to multiple mycotoxins, even at subclinical doses, had a negative effect on microbiota composition and microbiota-related metabolic functions. However, mycotoxin concentration within the gut varies considerably due to bioavailability, excretion, the effect of the microbiota on mycotoxins, as well as which segment of the gut is being analyzed. Analyzing the different parts of the gut microbiome profile in response to FUM and DON exposure would provide a clearer picture of the impact of mycotoxins on the gut microbiome.

Technical Abstract: Fusarium toxins are one of the most common contaminants in poultry diets. Cooccurrence of fumonisins (FUM) and deoxynivalenol (DON), even at a subclinical dose, negatively affects the growth performance, intestinal integrity and induce subclinical necrotic enteritis in broiler chickens. Loss of gut integrity can be expected to alter the intestinal microbiota composition. The objective of this study was to identify the effects of combined FUM and DON on the cecal microbiome profile and predicted metabolic functions and short chain fatty acid profile in broilers challenged with Clostridium perfringens. A total of 240 one-day-old chicks were randomly assigned to two treatments, a control diet and or the control diet with 3mg/kg FUM + 4 mg/kg DON each with eight replications. All the birds were received cocci vaccine at d0. All birds in both treatment groups were challenged with C. perfringens 1 X 108 CFU via feed on d19 and 20 to achieve 5% mortality. On d35, FUM and DON contaminated diet numerically (P= 0.06) decreased the body weight gain by 84g compared to the control group. The bacterial compositions of the cecal contents were analyzed by sequencing the V3–V4 region of the 16S rRNA gene. Overall, microbial richness and diversity increased (P < 0.02) during the studied period (d 21 – 35). Cecal contents of birds in the FUM + DON group had greater (P < 0.05) microbial evenness and diversity (Shannon index), compared to the control group. FUM + DON exposure decreased (P = 0.001) the relative abundance of Proteobacteria in the cecal content, compared to the control group. The abundance of Defluviitaleaceae and Lachnospiraceae families were lower (P < 0.05) in the ceca of control group birds, but the abundances of Moraxellaceae and Streptococcaceae were higher (P < 0.05). At the genus level, FUM + DON exposure decreased (P < 0.05) Acinetobacter and Pseudomonas abundance and had a tendency (P = 0.08) to decrease Thermincola abundance, compared to the control group. In the ileum, no NE-specific microscopic abnormalities were found however tip of the ileal villi was compromised. The present findings showed that dietary FUM and DON contamination, even at subclinical levels, dysregulated intestinal functions and impaired the gut immune response, which potentially predisposing the birds to necrotic enteritis.