Abstract
This study aimed to investigate the effects of replacing of dietary inorganic iron with iron-rich Lactobacillus plantarum and iron-rich Candida utilis on the growth performance, serum parameters, immune function and iron metabolism of weaned piglets. Fifty-four 28-day-old healthy Duroc × Landrace × Yorkshire castrated male weanling piglets of similar body weight were randomly and equally divided into three groups. The piglets were kept in three pens per group, with six pigs in each pen. The dietary treatments were (1) a basal diet + ferrous sulfate preparation containing 120 mg/kg iron (CON); (2) a basal diet + iron-rich Candida utilis preparation containing 120 mg/kg iron (CUI); and (3) a basal diet + iron-rich Lactobacillus plantarum preparation containing 120 mg/kg iron (LPI). The entire feeding trial lasted for 28 days, after which blood, viscera, and intestinal mucosa were collected. The results showed no significant difference in growth parameters and organ indices of the heart, liver, spleen, lung, and kidney of weaned piglets when treated with CUI and LPI compared with the CON group (P > 0.05). However, CUI and LPI significantly reduced the serum contents of AST, ALP, and LDH (P < 0.05). Serum ALT content was significantly lower in the LPI treatment compared to the CON group (P < 0.05). Compared to CON, CUI significantly increased the contents of serum IgG and IL-4 (P < 0.05), and CUI significantly decreased the content of IL-2. LPI significantly increased the contents of serum IgA, IgG, IgM and IL-4 (P < 0.05), while LPI significant decreased the levels of IL-1β, IL-2, IL-6, IL-8, and TNF-α compared to CON (P < 0.05). CUI led to a significant increase in ceruloplasmin activity and TIBC (P < 0.05). LPI significantly increased the contents of serum Fe and ferritin, and increased the serum ceruloplasmin activity and TIBC compared to CON (P < 0.05). Furthermore, CUI resulted in a significant increase in the relative mRNA expression of FPN1 and DMT1 in the jejunal mucosa (P < 0.05). LPI significantly increased the relative mRNA expression of TF, FPN1, and DMT1 in the jejunal mucosa (P < 0.05). Based on these results, the replacement of dietary inorganic iron with an iron-rich microbial supplement could improve immune function, iron absorption and storage in piglets.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11259-023-10162-6/MediaObjects/11259_2023_10162_Figa_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11259-023-10162-6/MediaObjects/11259_2023_10162_Figb_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11259-023-10162-6/MediaObjects/11259_2023_10162_Figc_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11259-023-10162-6/MediaObjects/11259_2023_10162_Figd_HTML.jpg)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11259-023-10162-6/MediaObjects/11259_2023_10162_Fig5_HTML.png)
Similar content being viewed by others
Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Anderson GJ, Frazer DM (2017) Current understanding of iron homeostasis. Am J Clin Nutr 106. https://doi.org/10.3945/ajcn.117.155804. :1559S-1566S
Axling U, Önning G, Combs MA, Bogale A, Högström M, Svensson M (2020) The effect of Lactobacillus plantarum 299v on Iron Status and physical performance in female Iron-deficient athletes: a Randomized Controlled Trial. Nutrients 12. https://doi.org/10.3390/nu12051279
Bampidis V, Azimonti G, Bastos MdL, Christensen H, Dusemund B, Kouba M, Kos Durjava M, López-Alonso M, López Puente S, Marcon F, Mayo B, Pechová A, Petkova M, Sanz Y, Villa RE, Woutersen R, Cubadda F, Flachowsky G, Mantovani A, López-Gálvez G, Ramos F (2019) Safety and efficacy of iron chelates of lysine and glutamic acid as feed additive for all animal species. EFSA J 17:e05792. https://doi.org/10.2903/j.efsa.2019.5792
Borchers AT, Selmi C, Meyers FJ, Keen CL, Gershwin ME (2009) Probiotics and immunity. J Gastroenterol 44:26–46. https://doi.org/10.1007/s00535-008-2296-0
Byrne L, Murphy RA (2022) Relative bioavailability of Trace Minerals in Production Animal Nutrition: a review. Anim (Basel) 12. https://doi.org/10.3390/ani12151981
Camaschella C (2019) Iron deficiency. Blood 133:30–39. https://doi.org/10.1182/blood-2018-05-815944
Chen X, Zhang X, Zhao J, Tang X, Wang F, Du H (2019) Split iron supplementation is beneficial for newborn piglets. Biomed Pharmacother 120:109479. https://doi.org/10.1016/j.biopha.2019.109479
Chen S, Wu X, Wang X, Shao Y, Tu Q, Yang H, Yin J, Yin Y (2020) Responses of intestinal microbiota and immunity to increasing dietary levels of Iron using a Piglet Model. Front Cell Dev Biol 8:603392. https://doi.org/10.3389/fcell.2020.603392
Cortes-Perez NG, de Moreno LeBlanc A, Gomez-Gutierrez JG, LeBlanc JG, Bermúdez-Humarán LG (2021) Probiotics and trained immunity. https://doi.org/10.3390/biom11101402. Biomolecules 11
Cui K, Wang Q, Wang S, Diao Q, Zhang N (2019) The facilitating effect of Tartary Buckwheat Flavonoids and Lactobacillus plantarum on the growth performance, nutrient digestibility, antioxidant capacity, and fecal microbiota of weaned piglets. Anim (Basel) 9. https://doi.org/10.3390/ani9110986
Das NK, Schwartz AJ, Barthel G, Inohara N, Liu Q, Sankar A, Hill DR, Ma X, Lamberg O, Schnizlein MK, Arqués JL, Spence JR, Nunez G, Patterson AD, Sun D, Young VB, Shah YM (2020) Microbial Metabolite Signaling is required for systemic Iron homeostasis. Cell Metab 31:115–130e6. https://doi.org/10.1016/j.cmet.2019.10.005
Ding H, Yu X, Feng J (2020) Iron homeostasis disorder in piglet intestine. Metallomics 12:1494–1507. https://doi.org/10.1039/d0mt00149j
Dong Z, Wan D, Yang H, Li G, Zhang Y, Zhou X, Wu X, Yin Y (2020) Effects of Iron Deficiency on serum metabolome, hepatic histology, and function in neonatal piglets. Anim (Basel) 10. https://doi.org/10.3390/ani10081353
Dong Z, Zhang D, Wu X, Yin Y, Wan D (2022) Ferrous Bisglycinate Supplementation modulates intestinal antioxidant capacity via the AMPK/FOXO pathway and reconstitutes gut microbiota and bile acid profiles in Pigs. J Agric Food Chem 70:4942–4951. https://doi.org/10.1021/acs.jafc.2c00138
Feng X, Jiang S, Zhang F, Wang R, Zhao Y, Zeng M (2019) Siderophore (from Synechococcus sp. PCC 7002)-Chelated Iron promotes Iron Uptake in Caco-2 cells and ameliorates Iron Deficiency in rats. Mar Drugs 17. https://doi.org/10.3390/md17120709
Ghasemi HA, Hajkhodadadi I, Hafizi M, Taherpour K, Nazaran MH (2020) Effect of advanced chelate technology based trace minerals on growth performance, mineral digestibility, tibia characteristics, and antioxidant status in broiler chickens. Nutr Metab (Lond) 17:94. https://doi.org/10.1186/s12986-020-00520-5
Gulec S, Anderson GJ, Collins JF (2014) Mechanistic and regulatory aspects of intestinal iron absorption. Am J Physiol Gastrointest Liver Physiol 307:G397–409. https://doi.org/10.1152/ajpgi.00348.2013
Håkenåsen IM (2017) Feed intake, nutrient digestibility, growth performance and general health of piglets fed increasing levels of yeast. Norwegian University of Life Sciences
Hoppe M, Önning G, Hulthén L (2017) Freeze-dried Lactobacillus plantarum 299v increases iron absorption in young females-double isotope sequential single-blind studies in menstruating women. PLoS ONE 12:e0189141. https://doi.org/10.1371/journal.pone.0189141
Hu P, Mao J, Zeng Y, Sun Z, Deng H, Chen C, Sun W, Tang Z (2022) Isolation, identification, and function of Rhodotorula mucilaginosa TZR2014 and its Effects on the growth and health of weaned piglets. Front Microbiol 13:922136. https://doi.org/10.3389/fmicb.2022.922136
Huynh U, Qiao M, King J, Trinh B, Valdez J, Haq M, Zastrow ML (2022) Differential Effects of Transition Metals on Growth and Metal Uptake for two distinct Lactobacillus species. Microbiol Spectr 10:e0100621. https://doi.org/10.1128/spectrum.01006-21
Kim JH, Da Kim H, Jo S, Cho MJ, Cho YR, Lee YJ, Byun S (2022) Immunomodulatory functional foods and their molecular mechanisms. Exp Mol Med 54:1–11. https://doi.org/10.1038/s12276-022-00724-0
Liu L, Chen D, Yu B, Luo Y, Huang Z, Zheng P, Mao X, Yu J, Luo J, Yan H, He J (2021) Influences of selenium-enriched yeast on growth performance, Immune function, and antioxidant capacity in weaned Pigs exposure to oxidative stress. Biomed Res Int 2021:5533210. https://doi.org/10.1155/2021/5533210
Ma Y, Sun Z, Zeng Y, Hu P, Sun W, Liu Y, Hu H, Rao Z, Tang Z (2021) Isolation, identification and function of Pichia anomala AR2016 and its Effects on the Growth and Health of Weaned Pigs. Anim (Basel) 11. https://doi.org/10.3390/ani11041179
Ma J, Duan Y, Li R, Liang X, Li T, Huang X, Yin Y, Yin J (2022) Gut microbial profiles and the role in lipid metabolism in shaziling pigs. Anim Nutr 9:345–356. https://doi.org/10.1016/j.aninu.2021.10.012
Mahroum N, Alghory A, Kiyak Z, Alwani A, Seida R, Alrais M, Shoenfeld Y (2022) Ferritin - from iron, through inflammation and autoimmunity, to COVID-19. J Autoimmun 126:102778. https://doi.org/10.1016/j.jaut.2021.102778
Männer K, Lester H, Henriquez-Rodriguez E (2021) Ferric citrate is a safe and digestible source of iron in broilers and piglets. PeerJ 9:e12636. https://doi.org/10.7717/peerj.12636
National Research Council. (2012). Nutrient requirements of swine.
Nishito Y, Kambe T (2018) Absorption mechanisms of Iron, copper, and zinc: an overview. J Nutr Sci Vitaminol (Tokyo) 64:1–7. https://doi.org/10.3177/jnsv.64.1
Nowosad K, Sujka M, Pankiewicz U, Miklavčič D, Arczewska M (2021) Pulsed Electric Field (PEF) enhances Iron Uptake by the yeast Saccharomyces cerevisiae. https://doi.org/10.3390/biom11060850. Biomolecules 11
Núñez MT (2010) Regulatory mechanisms of intestinal iron absorption-uncovering of a fast-response mechanism based on DMT1 and ferroportin endocytosis. BioFactors 36:88–97. https://doi.org/10.1002/biof.84
Piskin E, Cianciosi D, Gulec S, Tomas M, Capanoglu E (2022) Iron absorption: factors, Limitations, and improvement methods. ACS Omega 7:20441–20456. https://doi.org/10.1021/acsomega.2c01833
Prabhakar PK (2020) Bacterial siderophores and their potential applications: a review. Curr Mol Pharmacol 13:295–305. https://doi.org/10.2174/1874467213666200518094445
Pu Y, Li S, **ong H, Zhang X, Wang Y, Du H (2018) Iron promotes Intestinal Development in neonatal piglets. https://doi.org/10.3390/nu10060726. Nutrients 10
Rusu IG, Suharoschi R, Vodnar DC, Pop CR, Socaci SA, Vulturar R, Istrati M, Moroșan I, Fărcaș AC, Kerezsi AD, Mureșan CI, Pop OL (2020) Iron supplementation influence on the Gut Microbiota and Probiotic Intake Effect in Iron Deficiency-A Literature-Based review. Nutrients 12. https://doi.org/10.3390/nu12071993
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int 23:3984–3999. https://doi.org/10.1007/s11356-015-4294-0
Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F (2011) Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14:403–414. https://doi.org/10.1016/j.cmet.2011.07.012
Sun J, Xu S, Du Y, Yu K, Jiang Y, Weng H, Yuan W (2022) Accumulation and Enrichment of Trace elements by yeast cells and their applications: a critical review. Microorganisms 10. https://doi.org/10.3390/microorganisms10091746
Vonderheid SC, Tussing-Humphreys L, Park C, Pauls H, OjiNjideka Hemphill N, LaBomascus B, McLeod A, Koenig MD (2019) A systematic review and Meta-analysis on the Effects of Probiotic Species on Iron absorption and Iron status. https://doi.org/10.3390/nu11122938. Nutrients 11
Wan D, Wu Q, Ni H, Liu G, Ruan Z, Yin Y (2019) Treatments for Iron Deficiency (ID): prospective Organic Iron Fortification. Curr Pharm Des 25:325–332. https://doi.org/10.2174/1381612825666190319111437
Wang H, Kim I-H (2021) Evaluation of Dietary Probiotic (Lactobacillus plantarum BG0001) supplementation on the growth performance, Nutrient Digestibility, Blood Profile, Fecal Gas Emission, and fecal microbiota in Weaning Pigs. Anim (Basel) 11. https://doi.org/10.3390/ani11082232
Wang D, Pu L, Wei G (2020) Improved antioxidant capacity and Immune function of broiler chickens Fed with Selenium-enriched Candida utilis. Braz J Poult Sci 22. https://doi.org/10.1590/1806-9061-2019-1047
Wu Y, Zhao J, Xu C, Ma N, He T, Zhao J, Ma X, Thacker PA (2020) Progress towards pig nutrition in the last 27 years. J Sci Food Agric 100:5102–5110. https://doi.org/10.1002/jsfa.9095
**e C, Elwan HAM, Elnesr SS, Dong X, Feng J, Zou X-T (2019) Effects of iron glycine chelate on laying performance, antioxidant activities, serum biochemical indices, iron concentrations and transferrin mRNA expression in laying hens. J Anim Physiol Anim Nutr (Berl) 103:547–554. https://doi.org/10.1111/jpn.13061
Yang Z, Wang Y, He T, Ziema Bumbie G, Wu L, Sun Z, Sun W, Tang Z (2021) Effects of Dietary Yucca Schidigera Extract and oral Candida utilis on Growth Performance and Intestinal Health of Weaned Piglets. Front Nutr 8:685540. https://doi.org/10.3389/fnut.2021.685540
Yang KM, Zhu C, Wang L, Cao ST, Yang XF, Gao KG, Jiang ZY (2021) Early supplementation with Lactobacillus plantarum in liquid diet modulates intestinal innate immunity through toll-like receptor 4-mediated mitogen-activated protein kinase signaling pathways in young piglets challenged with Escherichia coli K88. J Anim Sci 99(6):skab128. https://doi.org/10.1093/jas/skab128
Zhang R, Zhou M, Tu Y, Zhang NF, Deng KD, Ma T, Diao QY (2016) Effect of oral administration of probiotics on growth performance, apparent nutrient digestibility and stress-related indicators in Holstein calves. J Anim Physiol Anim Nutr (Berl) 100:33–38. https://doi.org/10.1111/jpn.12338
Zhang W-F, Tian M, Song J-S, Chen F, Lin G, Zhang S-H, Guan W-T (2021a) Effect of replacing inorganic trace minerals at lower organic levels on growth performance, blood parameters, antioxidant status, immune indexes, and fecal mineral excretion in weaned piglets. Trop Anim Health Prod 53:121. https://doi.org/10.1007/s11250-021-02561-1
Zhang X-G, Wang N, Ma G-D, Liu Z-Y, Wei G-X, Liu W-J (2021b) Preparation of S-iron-enriched yeast using siderophores and its effect on iron deficiency anemia in rats. Food Chem 365:130508. https://doi.org/10.1016/j.foodchem.2021.130508
Zhou Y, Wang B, Wang Q, Tang L, Zou P, Zeng Z, Zhang H, Gong L, Li W (2021) Protective Effects of Lactobacillus plantarum Lac16 on Clostridium perfringens Infection-Associated Injury in IPEC-J2 cells. Int J Mol Sci 22. https://doi.org/10.3390/ijms222212388
Acknowledgements
We thank Home for Researchers editorial team (www.home-for-researchers.com) for language editing service.
Funding
This work was supported by the Natural Science Foundation Project of Hunan (2022JJ30353).
Author information
Authors and Affiliations
Ethics declarations
Competing interests
The authors declare no competing interests.
Institutional Review Board Statement
The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the License of Experimental Animals (202103) of the Animal Experimentation Ethics Committee of Hunan Institute of Microbiology, Changsha, China.
Informed consent
Not applicable.
Conflict of interest
The authors declare no real or perceived conflicts of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zeng, Y., Yin, H., Zhou, X. et al. Effect of replacing inorganic iron with iron-rich microbial preparations on growth performance, serum parameters and iron metabolism of weaned piglets. Vet Res Commun 47, 2017–2025 (2023). https://doi.org/10.1007/s11259-023-10162-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-023-10162-6