Effects of altering the ratio of C16:0 and cis-9 C18:1 in rumen bypass fat on growth performance, lipid metabolism, intestinal barrier, cecal microbiota, and inflammation in fattening bulls

Abstract

Background: C16:0 and cis-9 C18:1 may have different effects on animal growth and health due to unique metabolism in vivo. This study was investigated to explore the different effects of altering the ratio of C16:0 and cis-9 C18:1 in fat supplements on growth performance, lipid metabolism, intestinal barrier, cecal microbiota, and inflammation in fattening bulls. Thirty finishing Angus bulls (626 ± 69 kg, 21 ± 0.5 months) were divided into 3 treatments according to the randomized block design: (1) control diet without additional fat (CON), (2) CON + 2.5% palmitic acid calcium salt (PA, 90% C16:0), and (3) CON + 2.5% mixed fatty acid calcium salt (MA, 60% C16:0 + 30% cis-9 C18:1). The experiment lasted for 104 d, after which all the bulls were slaughtered and sampled for analysis.

Results: MA tended to reduce 0-52 d dry matter intake compared to PA (DMI, P = 0.052). Compared with CON and MA, PA significantly increased 0-52 d average daily gain (ADG, P = 0.027). PA tended to improve the 0-52 d feed conversion rate compared with CON (FCR, P = 0.088). Both PA and MA had no significant effect on 52-104 days of DMI, ADG and FCR (P > 0.05). PA tended to improve plasma triglycerides compared with MA (P = 0.077), significantly increased plasma cholesterol (P = 0.002) and tended to improve subcutaneous adipose weight (P = 0.066) when compared with CON and MA. Both PA and MA increased visceral adipose weight compared with CON (P = 0.021). Only PA increased the colonization of Rikenellaceae, Ruminococcus and Proteobacteria in the cecum, and MA increased Akkermansia abundance (P < 0.05). Compared with CON, both PA and MA down-regulated the mRNA expression of Claudin-1 in the jejunum (P < 0.001), increased plasma diamine oxidase (DAO, P < 0.001) and lipopolysaccharide (LPS, P = 0.045). Compared with CON and MA, PA down-regulated the ZO-1 in the jejunum (P < 0.001) and increased plasma LPS-binding protein (LBP, P < 0.001). Compared with CON, only PA down-regulated the Occludin in the jejunum (P = 0.013). Compared with CON, PA and MA significantly up-regulated the expression of TLR-4 and NF-κB in the visceral adipose (P < 0.001) and increased plasma IL-6 (P < 0.001). Compared with CON, only PA up-regulated the TNF-α in the visceral adipose (P = 0.01). Compared with CON and MA, PA up-regulated IL-6 in the visceral adipose (P < 0.001), increased plasma TNF-α (P < 0.001), and reduced the IgG content in plasma (P = 0.035). Compared with CON, PA and MA increased C16:0 in subcutaneous fat and longissimus dorsi muscle (P < 0.05), while more C16:0 was also deposited by extension and desaturation into C18:0 and cis-9 C18:1. However, neither PA nor MA affected the content of cis-9 C18:1 in longissimus dorsi muscle compared with CON (P > 0.05).

Conclusions: MA containing 30% cis-9 C18:1 reduced the risk of high C16:0 dietary fat induced subcutaneous fat obesity, adipose tissue and systemic low-grade inflammation by accelerating fatty acid oxidative utilization, improving colonization of Akkermansia, reducing intestinal barrier damage, and down-regulating NF-κB activation.

Keywords: cis-9 C18:1; C16:0; Finishing bulls; Intestinal homeostasis; Lipid metabolism; Low-grade inflammation.

Fig. 1

Effects of dietary fat with different FA on α-diversity and β-diversity of cecal microbiota of finishing bulls (n = 6). A OTU Venn; B Rarefaction curve-Chao1; C β-diversity-PCoA analysis (3D); D β-diversity-PCoA analysis (2D). CON: control diet without additional fat; PA: CON + 2.5% DM palmitic calcium salt (90% C16:0); MA: CON + 2.5% DM mixed FA calcium salt (60% C16:0 + 30% cis-9 C18:1)

Fig. 2

Effects of dietary fat with different FA on cecal microbiota composition at phylum and genus level of finishing bulls (n = 6). A The composition of microbiota at the phylum level; B The differences of microbiota at the phylum level; C Microbiota composition at the genus level. CON: control diet without additional fat; PA: CON + 2.5% DM palmitic calcium salt (90% C16:0); MA: CON + 2.5% DM mixed FA calcium salt (60% C16:0 + 30% cis-9 C18:1). ^a,b Bars with different letters differ significantly at P < 0.05. Data are expressed as means ± SEM

Fig. 3

Dietary fat with different FA differentially regulated cecal microbiota in beef cattle (n = 6). A Cladogram of LEfSe shows taxonomic profiling from the phylum to genus level, the yellow node represents no difference, but other color nodes represent significant difference; B Linear discriminant analysis (LDA) distribution, and the score > 3.8 means significant. CON: control diet without additional fat; PA: CON + 2.5% DM palmitic calcium salt (90% C16:0); MA: CON + 2.5% DM mixed FA calcium salt (60% C16:0 + 30% cis-9 C18:1)

Fig. 4

Effects of dietary fat with different FA on gut permeability and endotoxemia of finishing bulls (n = 10). A The relative mRNA expression of zonula occludens-1 (ZO-1), Occludin, Claudin-1, Tricellulin, E-cadherin; B Plasma diamine oxidase (DAO); C Plasma D-lactic acid; D Plasma lipopolysaccharide (LPS); E Plasma lipopolysaccharide-binding protein (LBP). CON: control diet without additional fat; PA: CON + 2.5% DM palmitic calcium salt (90% C16:0); MA: CON + 2.5% DM mixed FA calcium salt (60% C16:0 + 30% cis-9 C18:1).^a,b Bars with different letters differ significantly at P < 0.05, **Representing P < 0.05 in the box plot. Data are expressed as means ± SEM

Fig. 5

Effects of dietary fat with different FA on mRNA expression of inflammatory response gene in visceral adipose of finishing bulls (n = 10). TLR-4: Toll-like receptor 4; PPARγ: Peroxisome proliferator-activated receptor γ; NF-κB: Nuclear factor kappa B; TNF-α: Tumour necrosis factor-α; IL-1β: Interleukin-1β; IL-6: Interleukin-6; IL-10: Interleukin-10; MCP-1: Monocyte chemoattractant protein-1. CON: control diet without additional fat; PA: CON + 2.5% DM palmitic calcium salt (90% C16:0); MA: CON + 2.5% DM mixed FA calcium salt (60% C16:0 + 30% cis-9 C18:1). ^a,b Bars with different letters differ significantly at P < 0.05. Data are expressed as means ± SEM