Selenate and selenite affect ruminal metabolism of C18 unsaturated fatty acids and fatty acid composition of lamb tissues
Graphical abstract
Introduction
In ruminants, fats are metabolised in the rumen stomach compartment through lipolysis (LP) to free fatty acids (FA) and glycerol (Kairenius et al., 2018). Microbial LP is necessary for the initial step in ruminal biohydrogenation (BH) (Jenkins et al., 2008; Buccioni et al., 2012). Ruminal microbiota use the BH as a means of protection against toxicity of polyunsaturated FA (PUFA), especially highly unsaturated FA. The final product of ruminal BH of two main essential PUFA (i.e. linoleic acid (LA) and α-linolenic acid (LNA)) is stearic acid (C18:0). When the BH is not completed, plethora of intermediary products (mainly various isomers of conjugated linoleic acid (CLA) and conjugated linolenic acid (CLnA) (Białek et al., 2017)) arises and become available for deposition in rumen content and tissues of ruminants (Or-Rashid et al., 2007; Buccioni et al., 2012; Gudla et al., 2012).
Impairment of the BH may be a result of modification of composition of microorganism population colonizing rumen as well as their activity through dietary interventions, e.g. supplementation of ruminants’ diet with polyphenols and/or selenium (Se) (Vasta and Luciano, 2011; Navarro-Alarcon and Cabrera-Vique, 2008; Kišidayová et al., 2014). Earlier studies showed that ruminants’ diets enriched with inorganic forms of Se (like selenite or selenate) and organic forms of Se (e.g. selenized yeast containing Se-methionine and Se-cysteine) are able to change the profiles of FA in ruminal content (fluids and microbiota) and selected tissues of lambs (Gabryszuk et al., 2007; Krajewska et al., 2012; Czauderna et al., 2012, 2013, 2015; Miltko et al., 2016; Białek et al., 2018). Selenate (SeVI) and selenite (SeIV) are the two most common supplemental forms of Se for ruminants (Mainville et al., 2009). Comparing SeVI and SeIV, SeVI has higher bioavailability value using tissue uptake by ruminants. Nowadays, ruminants were offered diets enriched in organic forms of Se (usually selenized yeast). Numerous studies show that the available inorganic Se sources (like SeIV or SeVI) are poorly incorporated by ruminal microorganisms and tissues of ruminants compared to organic sources of Se (e.g. selenized yeast) (Whanger, 2004; Mainville et al., 2009; Kišidayová et al., 2014). On the other hand, SeIV and SeVI (the inorganic forms of Se) are more chemically stable in diets than selenized yeast (containing Se-methionine and Se-cysteine).
Different physiological effects were also previously reported for selenite (SeIV) and selenate (SeVI) – two most common inorganic chemical forms of Se. SeIV more rapidly than SeVI reacts with compounds containing thiol group(s) and as a result may stimulate the oxidation of glutathione in ruminal microbiota and lambs’ tissues and thus, decrease the cellular levels of glutathione (Pizzorno, 2014; Schiavon et al., 2016; Čobanová et al., 2017). The toxicity of SeIV is higher than SeVI (Biswas et al., 1999). When Se-compounds were fed to animals in low doses (< 1 µg Se/kg body weight), SeVI was bioaccumulated to the greater extent than SeIV and faster urinary excretion of SeVI as compared to SeIV was observed (Dael et al., 2001; Navarro-Alarcon and Cabrera-Vique, 2008). Also results of our previous studies indicated that SeIV or SeVI affected the levels of positional and geometric isomers of CLA, C18:1, C18:2, C18:3 and other unsaturated FA (UFA) in ruminal fluids and lambs’ tissues (Wasowska et al., 2006a; Czauderna et al., 2012, 2013, 2015; Miltko et al., 2016).
The yield of UFA microbial isomerisation and the BH to intermediates and final products are also affected by the level and the type of dietary FA (especially long-chain PUFA) (Wasowska et al., 2006b; Buccioni et al., 2012; Czauderna et al., 2012, 2015; Miltko et al., 2016). Considering the above, we hypothesised that addition of two inorganic chemical forms of Se to ruminal fluids enriched with LNA would modify the BH in incubated rumen fluid samples both in form- and dose dependent manner. Thus, the change in the concentration of intermediate products (like long-chain PUFA (LPUFA), precursors of CLA and isomers of conjugated FA (CFA) including CLnA and CLA) are also expected. Moreover, we hypothesized that results of above mentioned in vitro experiments will be reflected in vivo studies on lambs fed a diet with linseed oil (LO, dietary source of LNA) and inorganic Se-compounds (as SeIV or SeVI) by modification of the FA profile in selected tissues. We argued that the practical benefit of Se-compounds added to ruminal fluid or ovine diet is to increase concentrations of unsaturated fatty acids (UFA) by reducing the oxidative stress in ruminal microbiota and tissues of lambs, which may be beneficial in terms of animal well-being and from the consumer’ perspective.
Thus, the main aim of our study was to determine effects of SeIV and SeVI added to ovine ruminal fluids with LNA on the content of selected FA during in vitro incubation. The second goal of our study was to confirm the results of in vitro experiment during in vivo study on farm animal model by investigation the effects a diet enriched in 2 ppm Se (as SeVI) and LNA (derived from LO) on the content of FA, especially the BH products, in selected tissues of lambs. Our study evaluates the effects of two concentrations of SeIV and SeVIin vitro experiments; the higher concentration of SeIV and SeVI in incubated ruminal fluids is similar to the concentration of Se in the rumen of lamb fed with the diet enriched in 2 ppm Se as SeVI. SeVI will be added to the diets because SeVI is more efficiently incorporated by ruminal microbiota and tissues of lambs than SeIV.
Section snippets
Reagents and chemicals
A CLA isomer mixture (97–99%), trans10cis12CLA (t10c12CLA) (95–97%), and c9t11CLA (95–97%) were supplied by Larodan Fine Chemicals AB (Malmö, Sweden); other fatty acid methyl ester (FAME) standards and sodium selenate and sodium selenite were purchased from Sigma-Aldrich Co. (St. Louis, USA). Dichloromethane (DCM), NaOH, KOH, Na2SO4, and concentrated HCl were supplied by POCH S.A. (Gliwice, Poland). Linseed oil (LO) was provided by APA Polska (Kobylnica near Poznan, Poland). LO included the
Effect of LNA without or with Se on contents of selected FA in incubated ruminal fluids
Our study showed that SeIV and SeVI added to ruminal fluids with LNA changed the contents of FA, especially UFA, in incubated fluid compared with the control ruminal fluids (RF) and incubated fluid containing only LNA (Tables 2 and 3). The levels of TVA in fluids containing LNA and the lower content of SeVI were higher (P ≤ 0.05) for incubation at all times from 18 h compared with the RF and all other supplemented ruminal fluids (Table 2). Detailed statistical analyses showed that there were
Discussion
Nowadays natural strategies of enrichment of food products in bioactive compounds are gaining importance in all agricultural branches. For animal breeders the most common, the simplest and the cheapest way of producing e.g. milk, meat and eggs with increased content of health-promoting substances is modification of animal feeding. Although in monogastric animals (like pigs or poultry) the enhancement of edible parts of carcass in nutritionally valuable compounds is relatively easy, in ruminants
Conclusion
The main novelty of our studies was to investigate the influence of two inorganic forms of Se added to ovine ruminal fluids with LNA on the profiles of FA (especially n-3LPUFA and CLA isomers) and the yield of the bacterial isomerisation and BH in both in vitro and in vivo experiments. SeVI supplementation reduced the BH capacity in the lambs’ rumen. As expected, SeVI added to the lambs diets with LO decreased the concentration of saturated fatty acids (like C18:0) in the liver and MBF.
CRediT authorship contribution statement
Małgorzata Białek: Software, Validation, Formal analysis, Investigation, Data curation. Marian Czauderna: Funding acquisition, Project administration, Supervision, Writing - original draft, Writing - review & editing, Conceptualization, Methodology. Wiesław Przybylski: Visualization, Software, Data curation, Software, Validation. Danuta Jaworska: Formal analysis, Investigation, Data curation, Validation.
Declaration of Competing Interest
The authors have declared that there are no conflicts of interest associated with this publication. All authors: Małgorzata Białek and Marian Czauderna have declared no conflict of interest. Moreover, all Authors have read the manuscript and have agreed to submit it in its current form for consideration for publication in the Journal.
Acknowledgements
This study was supported by the National Science centre: Grant No. 2013/09/B/ NZ9/00291 and by the statutory funds from the Kielanowski Institute of Animal Physiology and Nutrition, PAS (Poland). We thank Mrs. A. Kaszuba-Długosz and Mrs. G. Oktaba for technical help.
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