Abstract
Lipid metabolism can influence host’s health. There is increasing evidence for interplay between two key regulating factors in lipid metabolism: bile acids (BAs) and gut microbiota. However, very little is known about how types of different diet-supplemented bile salts (BS) influence this interaction in vivo. We sought to explore these relationships using grass carp (Ctenopharyngodon idellus), which often suffers functional disorder of liver and gallbladder. We studied fluctuations of BAs in the gall and changes of microbial communities in the gut in response to seven different diets: five different BS, chelating BS agent, and control. The BS comprised two primary BS [sodium taurochololate (TCAS) and sodium taurochenodeoxycholate (TCDCAS)], sodium tauroursodeoxycholate (TUDCAS), and two secondary BS [sodium taurodeoxycholate (TDCAS) and sodium taurolithocholate (TLCAS)]. Supplementation of primary BS caused a more significant fluctuation of biliary BAs than secondary BS, and TCAS caused a more prominent increase than TCDCAS and TUDCAS. For the gut microbiota, primary BS tended to increase their diversity and induce community succession, secondary BS resulted in a higher firmicutes/bacteroidetes ratio, while TUDCAS had no significant effects. Changes of the gut microbiota triggered by different types of BS caused alteration in BAs biotransformation. Two-obesity-associated families, Lachnospiraceae and Ruminococcaceae were positively correlated with biliary cholic acid (CA), taurochenodeoxycholic acid (TCDCA), and deoxycholic acid (DCA). As both primary and secondary BS resulted in increased synthesis of toxic secondary Bas by the gut microbiota, future studies should pay closer attention to gut microbiota when considering BA treatment.
Highlights
Lipid metabolism has a role in host’s health
bile acids (BAs) in the gallbladder of grass carp were dominated by cholic acid (CA) (1.0–120.1 ng/μl over groups) and tauroursodeoxycholic acid (TUDCA) (3.6–86.1 ng/μl over all groups), followed by medium levels of chenodeoxycholic acid (CDCA) (0.1–4.1 ng/μl over groups), taurochenodeoxycholic acid (TCDCA) (0–9.3 ng/μl over groups), and deoxycholic acid (DCA) (0–9.1 ng/μl over groups), and low levels of taurocholic acid (TCA) (0–0.4 ng/μl over groups), taurodeoxycholic acid (TDCA) (0–0.6 ng/μl over groups), ursodeoxycholic acid (UDCA) (0–0.03 ng/μl over groups), lithocholic acid (LCA) (0–0.006 ng/μl over groups), and taurolithocholic acid (TLCA) (0–0.0001 ng/μl over groups) (Figure 1)
Compared with the Ctrl group, the concentration of total BAs in groups fed with primary bile salts (BS) (TCAS and TCDCAS) and TUDCAS showed significant increase, the groups fed with secondary BS (TDCAS and TLCAS) and chelating agent (Chol group) did not show significant increase (P < 0.05, Supplementary Table S1)
Summary
Lipid metabolism has a role in host’s health. Disorders of lipid metabolism lead to serious, sometimes life-threatening, health problems, including obesity, cardiovascular, and hepatobiliary diseases (Lee et al, 2003; Reddy and Rao, 2006). As bile acids (BAs) are known to play an important role in a large number of metabolic disorders (Hofmann and Hagey, 2014; Zhou and Hylemon, 2014), they have been recognized as a putatively important factor in this complex interplay (Yokota et al, 2012) They are synthetized from cholesterol in liver and secreted into the intestinal lumen as bile, where they help lipid digestion and absorption. Recent studies have demonstrated that gut microbiota have important roles in adjusting the levels and profiles of BAs in various tissues (e.g., liver, kidney, plasma, and heart) (Swann et al, 2011) In this regard, by altering the composition of BAs, gut microbiota has the potential to change host’s physiology and metabolism. Despite the importance of this issue, and different species of BAs could have completely distinct effects on host metabolism (Vallim et al, 2013), apart from two studies conducted on rats and mice with one species of BAs [cholic acid (CA)] supplemented in diet (Islam et al, 2011; Zheng et al, 2017), attempts to elucidate the effects of different dietary BAs on shaping the gut microbiota in vivo remain sparse
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