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Short-term dietary changes can result in mucosal and systemic immune depression.

ABSTRACT: Omnivorous animals, including mice and humans, tend to prefer energy-dense nutrients rich in fat over plant-based diets, especially for short periods of time, but the health consequences of this short-term consumption of energy-dense nutrients are unclear. Here, we show that short-term reiterative switching to 'feast diets', mimicking our social eating behavior, breaches the potential buffering effect of the intestinal microbiota and reorganizes the immunological architecture of mucosa-associated lymphoid tissues. The first dietary switch was sufficient to induce transient mucosal immune depression and suppress systemic immunity, leading to higher susceptibility to Salmonella enterica serovar Typhimurium and Listeria monocytogenes infections. The ability to respond to antigenic challenges with a model antigen was also impaired. These observations could be explained by a reduction of CD4⁺ T cell metabolic fitness and cytokine production due to impaired mTOR activity in response to reduced microbial provision of fiber metabolites. Reintroducing dietary fiber rewired T cell metabolism and restored mucosal and systemic CD4⁺ T cell functions and immunity. Finally, dietary intervention with human volunteers confirmed the effect of short-term dietary switches on human CD4⁺ T cell functionality. Therefore, short-term nutritional changes cause a transient depression of mucosal and systemic immunity, creating a window of opportunity for pathogenic infection.

SUBMITTER: Siracusa F

PROVIDER: S-EPMC10457203 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Short-term dietary changes can result in mucosal and systemic immune depression.

Siracusa Francesco F Schaltenberg Nicola N Kumar Yogesh Y Lesker Till R TR Steglich Babett B Liwinski Timur T Cortesi Filippo F Frommann Laura L Diercks Björn-Phillip BP Bönisch Friedericke F Fischer Alexander W AW Scognamiglio Pasquale P Pauly Mira J MJ Casar Christian C Cohen Yotam Y Pelczar Penelope P Agalioti Theodora T Delfs Flemming F Worthmann Anna A Wahib Ramez R Jagemann Bettina B Mittrücker Hans-Willi HW Kretz Oliver O Guse Andreas H AH Izbicki Jakob R JR Lassen Kara G KG Strowig Till T Schweizer Michaela M Villablanca Eduardo J EJ Elinav Eran E Huber Samuel S Heeren Joerg J Gagliani Nicola N

Nature immunology 20230814 9

Omnivorous animals, including mice and humans, tend to prefer energy-dense nutrients rich in fat over plant-based diets, especially for short periods of time, but the health consequences of this short-term consumption of energy-dense nutrients are unclear. Here, we show that short-term reiterative switching to 'feast diets', mimicking our social eating behavior, breaches the potential buffering effect of the intestinal microbiota and reorganizes the immunological architecture of mucosa-associate ...[more]

PMID: 37580603

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Project description:Immediate and short-term changes in diet composition can support individualized, real-time interventions in precision dairy production systems, and might increase feed efficiency (FE) of dairy cattle in the short-term. The objective of this study was to determine immediate and short-term effects of changes in diet composition on production parameters of dairy cattle fed varying amounts of top dressed commodities. A 4 × 4 replicated Latin square design was used to evaluate responses of twenty-four Holstein cows fed either no top dress (Control) or increasing amounts of: corn grain (CG), soybean meal (SBM), or chopped mixed grass hay (GH) top dressed on a total mixed ration (TMR) over four, 9-day periods. Throughout each period, top dressed commodities were incrementally increased, providing 0% to 20% of calculated net energy of lactation (NEL) intake. Measured production responses were analyzed for each 9-d period using a mixed-effects model considering two different time ranges. Samples collected from d 3 and 4 and from d 7 and 8 of each period were averaged and used to reflect "immediate" vs. "short-term" responses, respectively. In the immediate response time frame, control fed cows had lower milk yield, milk fat yield, and milk true protein yield than CG and SBM supplemented animals but similar responses to GH supplemented animals. Milk fat and protein percentages were not affected by top dress type in the immediate term. In the short-term response time-frame, GH supplemented animals had lower DMI and milk fat yield than all other groups. Control and GH supplemented cows had lower milk yield than CG and SBM fed cows. In the immediate response time frame, FE of SBM supplemented cows was superior to other groups. In the short-term time frame, FE of GH and SBM groups was improved over the control group. Results suggest that lactating dairy cows show rapid performance responses to small (<20% NEL) changes in dietary composition, which may be leveraged within automated precision feeding systems to optimize efficiency of production. Before this potential can be realized, further research is needed to examine integration of such strategies into automatic feeding systems and downstream impacts on individual animal FE and farm profitability.

Dataset Information

Short-term dietary changes can result in mucosal and systemic immune depression.

Publications

Short-term dietary changes can result in mucosal and systemic immune depression.

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