Sex-Based Differences in Gut Microbiota Composition in Response to Tuna Oil and Algae Oil Supplementation in a D-galactose-Induced Aging Mouse Model - PubMed (original) (raw)

doi: 10.3389/fnagi.2018.00187. eCollection 2018.

Zhaoyang Wang 1, Yanyan Li 2, Jiaojiao Han 1, Chenxi Cui 1, Chenyang Lu 1, Jun Zhou 1, Lingzhi Cheong 1, Ye Li 1, Tingting Sun 1, Dijun Zhang 1, Xiurong Su 1

Affiliations

Sex-Based Differences in Gut Microbiota Composition in Response to Tuna Oil and Algae Oil Supplementation in a D-galactose-Induced Aging Mouse Model

Hongyan Zhang et al. Front Aging Neurosci. 2018.

Abstract

Our previous work indicated that a mixture of tuna oil and algae oil treatment in male mice effectively relieved D-galactose (D-gal)-induced aging and resulted in gut microbiota alterations, and that the best anti-aging effects were observed for a tuna oil to algae oil ratio of 1:2. However, the possibility of a sex-based difference in the anti-aging effect of the tuna oil and algae oil mixture or gut microbiota variation, has rarely been investigated. In this study, the anti-aging effect of an oil mixture (1:2) in male and female mice was measured, and oil treatment improved the learning and cognition of mice that were damaged by D-gal, increased the activities of anti-oxidative enzymes, and decreased the level of MDA, which acted as a hallmark of oxidative damage to lipids. Male mice showed better anti-aging effects than female mice with a specific oil mixture ratio, and the clinical drug donepezil showed a similar or better effect on aging alleviation than oil treatments in both sexes. On the other hand, the same oil treatment led to different gut microbiota composition alterations in male and female mice. Redundancy analysis (RDA) identified 31 and 30 key operational taxonomic units (OTUs) in the male and female mice, respectively, and only three of these OTUs overlapped. Moreover, the abundance of Lactobacillus and several probiotic-like butyric acid producers was higher in male mice than in female mice, whereas the abundance of some inflammation-related genera, such as Clostridium XlVa, was lower in male mice. In conclusion, this study indicated the sex-based differences related to the anti-aging effects of tuna oil and algae oil treatment are accompanied by sex-based differences in gut microbiota modulation.

Keywords: aging; algae oil; gut microbiota; sex-based differences; tuna oil.

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Figures

Figure 1

Figure 1

Effects of oil treatment on body weight and brain index in female mice. (A) The relative body weight gain of D-galactose (D-gal)-treated mice with oil treatment. (B) Changes in the brain index of female mice that received oil treatment. The data are shown as the mean ± SEM, n = 12 per group. *P < 0.05, **P < 0.01 vs. D-gal group.

Figure 2

Figure 2

The effects of oil treatment on memory and spatial learning in D-gal-treated female mice. (A) Escape latency to the hidden platform on the 5th day. (B) The exact number of platform crossings on the 5th day. (C) A comparison of time spent in the target quadrant on the 5th day. (D) The swimming speeds on the 5th day. The data are shown as the mean ± SEM, n = 12 per group. *P < 0.05, **P < 0.01 vs. D-gal group.

Figure 3

Figure 3

Effects of D-gal, donepezil and oil treatments on malondialdehyde (MDA; A), Glutathione peroxidase (GSH-Px; B), superoxide dismutase (SOD; C), total anti-oxidant capacity (T-AOC; D) and catalase (CAT; E) in the brain. The data are shown as the mean ± SEM, n = 12 per group. *P < 0.05, **P < 0.01 vs. D-gal group.

Figure 4

Figure 4

The alpha diversity of the gut microbiota in the different groups of female and male mice. (A) Shannon index; (B) Simpson index. +P < 0.05, ++P < 0.01 and +++P < 0.001 vs. D-gal group in the male. #P < 0.05, ##P < 0.01 and ###P < 0.001 vs. D-gal group in the female. *P < 0.05, **P < 0.01 and ***P < 0.001, corresponding to the treatment group in male vs. female mice, and n = 3 per group.

Figure 5

Figure 5

Weighted UniFrac Principal co-ordinates (PCoA) analysis of the gut microbiota in male and female mice with different treatments.

Figure 6

Figure 6

The abundance of 58 operational taxonomic units (OTUs) was altered by D-gal and oil treatment based on redundancy analysis (RDA). (A) The heatmap for female mice. (B) The heatmap for male mice. The OTUs are sorted by phylogenetic position. The OTUs with higher abundance in females are labeled in red, whereas the OTUs with higher abundance in males are labeled in blue. Green represents the OTUs that were found in both sexes. The color of the heatmap represents the normalized relative abundance of the 58 OTUs. The taxonomy (genus) of the OTUs is at the right. The color of the squares represents the average abundance of the OTUs, and n = 3 per group.

Figure 7

Figure 7

The correlations between phenotypes and OTU abundance was obtained via SPSS in Spearman mode. (A) The correlation between females and males. Significant associations are marked with an asterisk *, *P < 0.05 and **P < 0.01. (B) The correlations between phenotypes and OTU abundance in females. (C) The correlations between phenotypes and OTU abundance in males. The OTUs are ordered by their phylogenetic positions, and the classification of each OUT’s genus is at the bottom.

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