Lowered dietary phosphorus affects intestinal and renal gene expression to maintain mineral homeostasis with immunomodulatory implications in weaned piglets

Abstract

BackgroundIn monogastric animals, phosphorus (P) homeostasis is maintained by regulating intestinal absorption, bone mobilization, and renal excretion. Since P is a non-renewable resource, a shortage is imminent due to widespread over-usage in the farming and animal husbandry industries. As a consequence, P efficiency should be improved in pig production. We sought to characterize the transcriptional response in re−/absorbing and excreting tissues in pigs to diets varying in calcium: phosphorus ratios. Weaned piglets were assigned to one of three groups fed diets varying in digestible P content for a period of five weeks. Gene expression profiles were analyzed in jejunum, colon, and kidney.ResultsTranscriptome analysis revealed that reduced dietary P intake affects gene expression in jejunum and kidney, but not in colon. The regulation of mineral homeostasis was reflected via altered mRNA abundances of CYP24A1, CYP27A1, TRPM6, SPP1, and VDR in jejunum and kidney. Moreover, lowered abundances of transcripts associated with the classical complement system pathway were observed in the jejunum. In kidney, shifted transcripts were involved in phospholipase C, calcium signaling, and NFAT signaling, which may have immunomodulatory implications.ConclusionsOur results revealed local transcriptional consequences of variable P intake in intestinal and renal tissues. The adaptive responses are the result of organismal efforts to maintain systemic mineral homeostasis while modulating immune features at local tissue sites. Therefore, the deviation from the currently recommended dietary P supply must be carefully considered, as the endogenous mechanisms that respond to low P diets may impact important adaptive immune responses.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4584-2) contains supplementary material, which is available to authorized users.

Bridging Gaps in the Agricultural Phosphorus Cycle from an Animal Husbandry Perspective—The Case of Pigs and Poultry

“…Moreover, the P homeostasis also depends on several sometimes contradictory factors such as regulators, transporters, and endocrine and paracrine signals whose endocrine function and integration into networks have not yet been clearly identified [20][21][22][23][24][25][26]. Consequently, the mechanisms that mediate P homeostasis contribute to a significant phenotypical variation [27,28]. Accordingly, one important step to improve P efficiency and reduce P excretion is a finely graduated phase feeding or precision feeding regimen which is already used to a certain extent to adapt growth performance to ontogenetic requirements.…”

“…Few studies with holistic approaches have focused on molecular metabolic pathways that are relevant for reduced and excessive P supply in farm animals [28,52]. Experiments elucidating the genotype-phenotype map will likely prove beneficial for the characterization of the molecular mechanisms of P efficiency.…”

“…Accordingly, as endogenous mechanisms affect important adaptive immune responses, research on P homeostasis requires considerable attention due to its importance in health and disease [57]. In pigs, interactions between the dietary P supply and the immune system can be deduced [28,58]. Hence, nutrition links the skeletal system with the immune system to a transdisciplinary field known as osteoimmunology [59,60].…”

Ileal Transcriptome Profiles of Japanese Quail Divergent in Phosphorus Utilization

“…Although one animal from the low PU group showed some uncertainty, successful discrimination of PU divergent animals based on ileal gene expression underlines the relevance of the intestinal capacity and the involvement of host genetic factors in the population-wide variability of PU as previously indicated by heritability estimates for this trait [5]. Accordingly, studies in non-avian monogastric species such as pigs revealed a gene-environment interaction in relation to P homeostasis [2,8,17]. Using the ileal DEGs, a functional enrichment analysis was performed to further clarify the underlying mechanisms and the intestinal contribution to PU.…”

“…Due to physiological turn-over and growth processes, the dynamics of P absorption, P storage, and P excretion are of particular importance to maintain animal health and growth performance. The resulting interaction of tissues such as small intestine, bones, and kidneys prompt an individual physiological release of hormones [1], tissue-specific downstream signaling events [2], and modified bone mineralization [3] to account for varying environmental conditions. With respect to P, physiologic adaptations imply effects on gastrointestinal processes, intermediate metabolism, and mechanisms of resource allocation, which all affect the efficiency of P utilization (PU) of the animal.…”