Dietary iron (Fe) influences manganese (Mn) utilization in chickens fed with inorganic Mn-supplemented diet. This study aimed to determine if dietary Fe levels affect Mn utilization in broilers fed with organic Mn-supplemented diet. Nine hundred 8-day-old broilers were randomly assigned to 1 of 6 treatments in a 3 (Fe level) × 2 (Mn source) factorial arrangement after feeding Mn- and Fe-unsupplemented diets for 7 days. The broilers were fed the basal diets (approximately 28 mg Mn/kg and 60 mg Fe/kg) supplemented with 0, 80, or 160 mg/kg Fe (L-Fe, M-Fe, or H-Fe), and 100 mg/kg Mn from Mn sulfate (MnSO4) or manganese-lysine chelate (MnLys) for 35 days. The H-Fe diet decreased (P < 0.05) body weight gain and feed intake as compared with L-Fe and M-Fe diets regardless of dietary Mn sources. Dietary Fe levels did not influence (P > 0.10) serum Mn concentration in MnLys-treated broilers, but serum Mn concentration decreased (P < 0.05) with dietary Fe increasing in MnSO4-treated broilers. The Mn concentration in the duodenum and tibia decreased (P < 0.05) with increasing dietary Fe levels regardless of dietary Mn sources, and MnLys increased (P < 0.04) these indices as compared with MnSO4. Dietary Fe levels did not significantly influence (P > 0.11) Mn concentration and activity and mRNA abundance of manganese-containing superoxide dismutase (MnSOD) in the heart of MnLys-treaded broilers, but the H-Fe diet decreased (P < 0.05) these indices in MnSO4-treated broilers as compared with M-Fe and L-Fe diets. The L-Fe diet increased (P < 0.001) duodenal divalent metal transporter 1 mRNA abundance when compared with the M-Fe and H-Fe diets on day 42, regardless of dietary Mn sources. The M-Fe and H-Fe diets decreased (P < 0.001) duodenal ferroportin 1 (FPN1) mRNA level when compared with the L-Fe diet in MnSO4-treated broilers, while dietary Fe levels did not significantly influence (P > 0.40) duodenal FPN1 mRNA abundance in MnLys-treated broilers. These results indicated dietary Fe levels decreased Mn utilization in MnSO4-treated broilers, but did not influence Mn utilization in MnLys-treated broilers evaluated by Mn concentrations in the serum and heart, and the activity and mRNA expression of heart MnSOD.
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Li L, Yang X (2018) The essential element manganese, oxidative stress, and metabolic diseases: links and interactions. Oxidative Med Cell Longev 2018:7580707. https://doi.org/10.1155/2018/7580707
Halpin KM, Baker DH (1986) Manganese utilization in the chick: effects of corn, soybean, fish meal, wheat bran, and rice bran on tissue uptake of manganese. Poult Sci 65:995–1003. https://doi.org/10.3382/ps.0650995
Henry PR (1995) Manganese bioavailability. In: Ammerman CB, Baker DH, Lewis AJ (eds) Bioavailability of nutrients for animals: amino acids, minerals, and vitamins. Academic Press, San Diego, pp 239–256
Bai SP, Lu L, Luo XG, Liu B (2008) Kinetics of manganese absorption in ligated small intestinal segments of broilers. Poult Sci 87:2596–2604. https://doi.org/10.3382/ps.2008-00117
Bai SP, Lu L, Wang RL, Xi L, Zhang LY, Luo XG (2012) Manganese source affects manganese transport and gene expression of divalent metal transporter 1 in the small intestine of broilers. Br J Nutr 108:267–276. https://doi.org/10.1017/S0007114511005629
Li X, Xie J, Lu L, Zhang L, Zou Y, Wang Q, Luo XG (2013) Kinetics of manganese transport and gene expressions of manganese transport carriers in Caco-2 cell monolayers. Biometals 26:941–953. https://doi.org/10.1007/s10534-013-9670-y
Ashmead HD (2001) The absorption and metabolism of iron amino acid chelate. Arch Latinoam Nutr 51(suppl 1):13–21
Ashmead HD (2012) Amino acid chelation in human and animal nutrition. CRC Press, Boca Raton
Zhang H, Gilbert ER, Zhang K, Ding X, Wang J, Zeng Q, Bai S (2016) Uptake of manganese from manganese-lysine chelate in the primary rat intestinal epithelial cells. J Anim Physiol Anim Nutr 101:147–158. https://doi.org/10.1111/jpn.12430
Davis CD, Wolf TL, Greger JL (1992) Varying levels of manganese and iron affect absorption and gut endogenous losses of manganese by rats. J Nutr 122:1300–1308. https://doi.org/10.1093/jn/122.6.1300
Thompson K, Molina R, Donaghey T, Brain JD, Wessling-Resnick M (2006) The influence of high iron diet on rat lung manganese absorption. Toxicol Appl Pharmacol 210:17–23. https://doi.org/10.1016/j.taap.2005.05.014
Hansen SL, Trakooljul N, Liu HC, Moeser AJ, Spears JW (2009) Iron transporters are differentially regulated by dietary iron, and modifications are associated with changes in manganese metabolism in young pigs. J Nutr 139:1474–1479. https://doi.org/10.3945/jn.109.105866
Bai S, Peng J, Zhang K, Ding X, Wang J, Zeng Q, Peng H, Bai J, Xuan Y, Su Z (2019) Effects of dietary iron on manganese utilization in broilers fed with corn-soybean meal diet. Biol Trace Elem Res:1–11. https://doi.org/10.1007/s12011-019-01780-w
Gunshin H, Allerson CR, Polycarpou-Schwarz M, Rofts A, Rogers JT, Kishi F, Hentze MW, Rouault TA, Andrews NC, Hediger MA (2001) Iron-dependent regulation of the divalent metal ion transporter. FEBS Lett 509:309–316. https://doi.org/10.1016/s0014-5793(01)03189-1
Thompson K, Molina RM, Donaghey T, Schwob JE, Brain JD, Wessling-Resnick M (2007) Olfactory uptake of manganese requires DMT1 and is enhanced by anemia. FASEB J 21:223–230. https://doi.org/10.1096/fj.06-6710com
Kim J, Li Y, Buckett PD, Bohlke M, Thompson KJ, Takahashi M, Maher TJ, Wessling-Resnick M (2012) Iron-responsive olfactory uptake of manganese improves motor function deficits associated with iron deficiency. PLoS One 7:e33533. https://doi.org/10.1371/journal.pone.0033533
Donovan A, Lima CA, Pinkus JL, Pinkus GS, Zon LI, Robine S, Andrews NC (2005) The iron exporter ferroportin/Slc40a is essential for iron homeostasis. Cell Metab 1:191–200. https://doi.org/10.1016/j.cmet.2005.01.003
Yin Z, Jiang H, Lee ES, Ni M, Erikson KM, Milatovic D, Bowman AB, Aschner M (2010) Ferroportin is a manganese-responsive protein that decreases manganese cytotoxicity and accumulation. J Neurochem 112:1190–1198. https://doi.org/10.1111/j.1471-4159.2009.06534.x
Madejczyk MS, Ballatori N (2012) The iron transporter ferroportin can also function as a manganese exporter. Biochim Biophys Acta 1818:651–657. https://doi.org/10.1016/j.bbamem.2011.12.002
Liao XD, Wang G, Lu L, Zhang LY, Lan YX, Li SF, Luo XG (2019) Effect of manganese source on manganese absorption and expression of related transporters in the small intestine of broilers. Poult Sci. https://doi.org/10.3382/ps/pez293
Ji F, Luo XG, Lu L, Liu B, Yu SX (2006) Effect of manganese source on manganese absorption by the intestine of broilers. Poult Sci 85:1947–1952. https://doi.org/10.1093/ps/85.11.1947
Ji F, Luo XG, Lu L, Liu B, Yu SX (2006) Effects of manganese sources and calcium on manganese uptake by in vitro everted gut sacs of broilers’ intestinal segments. Poult Sci 85:1217–1225. https://doi.org/10.1093/ps/85.7.1217
Li S, Luo X, Liu B, Crenshaw TD, Kuang X, Shao G, Yu S (2004) Use of chemical characteristics to predict the relative bioavailability of supplemental organic manganese sources for broilers. J Anim Sci 82:2352–2362. https://doi.org/10.2527/2004.8282352x
Li SF, Luo XG, Lu L, Crenshaw TD, Bu YQ, Liu B, Kuang X, Shao GZ, Yu SX (2005) Bioavailability of organic manganese sources in broilers fed high dietary calcium. Anim Feed Sci Technol 123-124:703–715. https://doi.org/10.1016/j.anifeedsci.2005.04.052
Luo XG, Li SF, Lu L, Liu B, Kuang X, Shao GZ, Yu SX (2007) Gene expression of manganese-containing superoxide dismutase as a biomarker of manganese bioavailability for manganese sources in broilers. Poult Sci 86:888–194. https://doi.org/10.1093/ps/86.5.888
Li SF, Luo XG, Lu L, Liu B, Kuang X, Shao GZ, Yu SX (2008) Effect of intravenously injected manganese on the gene expression of manganese-containing superoxide dismutase in broilers. Poult Sci 87:2259–2265. https://doi.org/10.3382/ps.2007-00525
Li S, Lin Y, Lu L, Xi L, Wang Z, Hao S, Zhang L, Li K, Luo X (2011) An estimation of the manganese requirement for broilers from 1 to 21 days of age. Biol Trace Elem Res 143:939–948. https://doi.org/10.1007/s12011-010-8931-7
National Research Council (1994) Nutrient requirements of poultry, 9th edn. The National Academy Press, Washington, DC
AOAC (2004) AOAC official methods of analysis, 15th edn. Association of Official Analytical Chemists, Washington DC
Chinese Industry Standard (NY/T 2694–2015) (2015) Determination of complexation (chelation) strengths of manganese-amio acids and manganese-proteinates as feed additives. The Ministry of the People’s Republic of China, Beijing, China
Bai S, Huang L, Luo Y, Wang L, Ding X, Wang J, Zeng Q, Zhang K (2014) Dietary manganese supplementation influences the expression of transporters involved in iron metabolism in chickens. Biol Trace Elem Res 160:352–360. https://doi.org/10.1007/s12011-014-0073-x
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 1(−Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Li S, Lu L, Hao S, Wang Y, Zhang L, Liu S, Liu B, Li K, Luo X (2011) Dietary manganese modulates expression of the manganese-containing superoxide dismutase gene in chickens. J Nutr 141:189–194. https://doi.org/10.3945/jn.110.126680
Wang F, Lu L, Li S, Zhang L, Yao J, Luo X (2012) Relative bioavailability of manganese proteinate for broilers fed a conventional corn-soybean meal diet. Bio Trace Elem Res 146:181–186. https://doi.org/10.1007/s12011-011-9238-z
Zhang H, Gilbert ER, Pan S, Zhang K, Ding X, Wang J, Zeng Q, Bai S (2016) Dietary iron concentration influences serum concentrations of manganese in rats consuming organic and inorganic sources of manganese. Br J Nutr 115:585–593. https://doi.org/10.1017/S0007114515004900
Akter M, Iji PA, Graham H (2017) Increased iron level in phytase-supplemented diets reduces performance and nutrient utilization in broiler chickens. Br Poult Sci 58:409–417. https://doi.org/10.1080/00071668.2017.1315050
Ma X, Liao X, Lu L, Li S, Zhang L, Luo X (2016) Determination of dietary iron requirements by full expression of iron-containing enzymes in various tissues of broilers. J Nutr 146:2267–2273. https://doi.org/10.3945/jn.116.237750
Liao X, Ma C, Lu L, Zhang L, Luo X (2017) Determination of dietary iron requirements by full expression of iron-containing cytochrome c oxidase in the heart of broilers from 22 to 42 d of age. Br J Nutr 118:493–499. https://doi.org/10.1017/S0007114517002458
Roth JA, Garrick MD (2003) Iron interactions and other biological reactions mediating the physiological and toxic actions of manganese. Biochem Pharmacol 66:1–13. https://doi.org/10.1016/s0006-2952(03)00145-x
Hansen SL, Ashwell MS, Moeser AJ, Fry RS, Knutson MD, Spears JW (2010) High dietary iron reduces transporters involved in iron and manganese metabolism and increases intestinal permeability in calves. J Dairy Sci 93:656–665. https://doi.org/10.3168/jds.2009-2341
Davis CD, Zech L, Greger JL (1993) Manganese metabolism in rats: an improved methodology for assessing gut endogenous losses. Proc Soc Exp Biol Med 202:103–108. https://doi.org/10.3181/00379727-202-43518
Malecki EA, Radzanowski GM, Radzanowski TJ, Gallaher DD, Greger JL (1996) Biliary manganese excretion in conscious rats is affected by acute and chronic manganese intake but not by dietary fat. J Nutr 126:489–498. https://doi.org/10.1093/jn/126.2.489
Gao T, Wang F, Li S, Luo X, Zhang X (2011) Manganese regulates manganese-containing superoxide dismutase (MnSOD) expression in the primary broiler myocardial cells. Biol Trace Elem Res 144:695–704. https://doi.org/10.1007/s12011-011-9093-y
Roth JA (2006) Homeostatic and toxic mechanisms regulating manganese uptake, retention, and elimination. Biol Res 39:45–57. https://doi.org/10.4067/s0716-97602006000100006
Davis CD, Ney DM, Gerger JL (1990) Manganese, iron and lipid interactions in rats. J Nutr 120:507–513. https://doi.org/10.1093/jn/120.5.507
Ye Q, Park JE, Gugnani K, Betharia S, Pino-Figueroa A, Kim J (2017) Influence of iron metabolism on manganese transport and toxicity. Metallomics 9:1028–1046. https://doi.org/10.1039/c7mt00079
Liu Y, Beyer A, Aebersold R (2016) On the dependency of cellular protein levels on mRNA abundance. Cell 165:535–550. https://doi.org/10.1016/j.cell.2016.03.014
The authors wish to thank Dr. Greg Fraley (Hope College, Holland, MI, USA) for the critical comments during the preparation of this manuscript.
This work was supported by the National Key Research and Development Program of China (2016YFD05005504), the National Natural Science Foundation of China (31001018), the Sichuan International Cooperation Project (2017HH0051), and the Chinese Chelota Group Research Project (2016LD0001).
All animal care and treatment procedures used in the current study were approved by the Animal Care and Use Committee of Sichuan Agricultural University.
The authors declare that they have no conflict of interest.
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Bai, S., Peng, J., Zhang, K. et al. Effects of Dietary Iron Concentration on Manganese Utilization in Broilers Fed with Manganese-Lysine Chelate-Supplemented Diet. Biol Trace Elem Res (2020) doi:10.1007/s12011-020-02035-9
- Organic manganese
- Manganese utilization
- Manganese-containing superoxide dismutase