Skip to main content
SpringerLink
Log in

Effects of Dietary Supplementation with κ-Selenocarrageenan on the Selenium Accumulation and Intestinal Microbiota of the Sea Cucumbers Apostichopus japonicus

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

A 30-day feeding trial was conducted to investigate the effect of κ-selenocarrageenan on the growth performance, selenium accumulation, antioxidant capacity, and intestinal microbiota of sea cucumbers Apostichopus japonicus, with different sizes (70 g ± 10 g and 100 g ± 10 g). Sea cucumbers of each size were randomly assigned into two groups; a diet without supplemented κ-selenocarrageenan was referred to as a control diet, or supplemented with κ-selenocarrageenan at selenium (Se) levels of 2.0 μg/g. Selenium accumulation in the body wall and intestine was determined on days 0, 10, 20, and 30. The survival rate (SR) was significantly higher in the κ-selenocarrageenan-treated group (Se group) than in the control group. After 30 days of feeding, κ-selenocarrageenan supplementation increased the activities of glutathione peroxidase (GSH-Px) and total antioxidant capacity (T-AOC), and decreased malondialdehyde (MDA) levels in A. japonicus. Furthermore, the intestinal microbiota diversity of sea cucumbers was increased by dietary supplementation with κ-selenocarrageenan and the relative abundances of some probiotics (such as Sulfitobacter and Rhodobacteraceae) were also increased. It is suggested that κ-selenocarrageenan could increase the antioxidant capacity and modulate the intestinal microbiota of sea cucumbers A. japonicus. Further researches will be conducted for its optimal administration concentrations in vivo.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Nan B, Min G (2017) Roles of zinc and selenium in protecting sea cucumber Apostichopus japonicus coelomocytes against lipopolysaccharide-induced oxidative stress in vitro. Aquac Res 48(4):1856–1865. https://doi.org/10.1111/are.13023

    Article  CAS  Google Scholar 

  2. Deng H, He C, Zhou Z, Liu C, Tan K, Wang N, Jiang B, Gao X, Liu W (2009) Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture 287(1-2):18–27. https://doi.org/10.1016/j.aquaculture.2008.10.015

    Article  CAS  Google Scholar 

  3. Liu H, Zheng F, Sun X, Hong X, Dong S, Wang B, Tang X, Wang Y (2010) Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol 105(3):236–242. https://doi.org/10.1016/j.jip.2010.05.016

    Article  PubMed  Google Scholar 

  4. Pohanka M (2013) Role of oxidative stress in infectious diseases. A review. Folia Microbiol 58(6):503–513. https://doi.org/10.1007/s12223-013-0239-5

    Article  CAS  Google Scholar 

  5. Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64(2):178–189. https://doi.org/10.1016/j.ecoenv.2005.03.013

    Article  CAS  PubMed  Google Scholar 

  6. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30. https://doi.org/10.1016/j.aquatox.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  7. Cui Y, Hou Z, Ren Y, Men X, Zheng B, Liu P, Xia B (2020) Effects of aerial exposure on oxidative stress, antioxidant and non-specific immune responses of juvenile sea cucumber Apostichopus japonicus under low temperature. Fish Shellfish Immunol 101:58–65. https://doi.org/10.1016/j.fsi.2020.03.050

    Article  CAS  PubMed  Google Scholar 

  8. Zenteno-Savín T, Saldierna R, Ahuejote-Sandoval M (2006) Superoxide radical production in response to environmental hypoxia in cultured shrimp. Comp Biochem Physiol Toxicol Pharmacol 142(3-4):301–308. https://doi.org/10.1016/j.cbpc.2005.11.001

    Article  CAS  Google Scholar 

  9. Elia AC, Prearo M, Pacini N, Dörr AJ, Abete MC (2011) Effects of selenium diets on growth, accumulation and antioxidant response in juvenile carp. Ecotoxicol Environ Saf 74(2):166–173. https://doi.org/10.1016/j.ecoenv.2010.04.006

    Article  CAS  PubMed  Google Scholar 

  10. Chen J, Han JH, Guan WT, Chen F, Wang CX, Zhang YZ, Lv YT, Lin G (2016) Selenium and vitamin E in sow diets: II. Effect on selenium status and antioxidant status of the progeny. Anim Feed Sci Technol 221:101–110. https://doi.org/10.1016/j.anifeedsci.2016.08.021

    Article  CAS  Google Scholar 

  11. Li MY, Gao CS, Du XY, Zhao L, Niu XT, Wang GQ, Zhang DM (2020) Effect of sub-chronic exposure to selenium and astaxanthin on Channa argus: bioaccumulation, oxidative stress and inflammatory response. Chemosphere 244:125546. https://doi.org/10.1016/j.chemosphere.2019.125546

    Article  CAS  PubMed  Google Scholar 

  12. Zhou N, Long H, Wang C, Yu L, Zhao M, Liu X (2020) Research progress on the biological activities of selenium polysaccharides. Food Funct 11(6):4834–4852. https://doi.org/10.1039/c9fo02026h

    Article  CAS  PubMed  Google Scholar 

  13. Jin W, Yu Y, Hou W, Wang G, Zhu Z, He J, Cheng S, Huang Q (2019) Molecular characteristics of kappa-selenocarrageenan and application in green synthesis of silver nanoparticles. Int J Biol Macromol 141:529–537. https://doi.org/10.1016/j.ijbiomac.2019.09.016

    Article  CAS  PubMed  Google Scholar 

  14. Wang JQ, Wang ZX, Zhang K, Zhang YM, Jiang YS, Liu CB, Yan-Qiang WU (2012) Effects of dietary selenomethionine levels on growth and some immune indices in juvenile sea cucumber Apostichopus japonicus. J Dalian Ocean Univ 27:110–115. https://doi.org/10.16535/j.cnki.dlhyxb.2012.02.009

    Article  Google Scholar 

  15. Xiao-Qian LU, Zhang M, Yang YU, Wang ZF, Yang S, Dang ZQ, Liu JB, Zhou W (2015) Effects of dietary selenium methionine on feeding and growth in juvenile sea cucumber Apostichopus japonicus. Chin J Fish 4:18–23

    Google Scholar 

  16. Zhou W, Cao Q, Wang ZF, Xiao-Jie HU, Zhang JY, Liu JB (2015) Effect of dietary methionine selenium on growth and digestive index of sea cucumber Apostichopus japonicus. J Dalian Ocean Univ 30:181–184. https://doi.org/10.3969/J.ISSN.2095-1388.2015.02.013

    Article  Google Scholar 

  17. Xiumei LI, Tao XU, Sun G, Yang J, Genrui LI, Haizhou LI (2017) Effects of dietary selenium-enriched yeast levels on important physiological enzymes and enrichment of selenium in sea cucumber (Apostichopus japonicus). Prog Fish Sci 38(4):155–163. https://doi.org/10.11758/yykxjz.20140512003

    Article  Google Scholar 

  18. Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242–249. https://doi.org/10.1038/nature11552

    Article  CAS  PubMed  Google Scholar 

  19. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, Codelli JA, Chow J, Reisman SE, Petrosino JF, Patterson PH, Mazmanian SK (2013) Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155(7):1451–1463. https://doi.org/10.1016/j.cell.2013.11.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Zhou L, Li H, Qin JG, Wang X, Chen L, Xu C, Li E (2020) Dietary prebiotic inulin benefits on growth performance, antioxidant capacity, immune response and intestinal microbiota in Pacific white shrimp (Litopenaeus vannamei) at low salinity. Aquaculture 518:734847. https://doi.org/10.1016/j.aquaculture.2019.734847

    Article  CAS  Google Scholar 

  21. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444(7122):1022–1023. https://doi.org/10.1038/4441022a

    Article  CAS  PubMed  Google Scholar 

  22. Wang J, Ren T, Han Y, Zhao Y, Liao M, Wang F, Jiang Z (2015) Effects of dietary vitamin C supplementation on lead-treated sea cucumbers, Apostichopus japonicus. Ecotoxicol Environ Saf 118:21–26. https://doi.org/10.1016/j.ecoenv.2015.04.009

    Article  CAS  PubMed  Google Scholar 

  23. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10(1):57–59. https://doi.org/10.1038/nmeth.2276

    Article  CAS  PubMed  Google Scholar 

  25. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  27. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41(Database issue):D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  28. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Han D, Xie S, Liu M, Xiao X, Liu H, Zhu X, Yang Y (2011) The effects of dietary selenium on growth performances, oxidative stress and tissue selenium concentration of gibel carp (Carassius auratus gibelio). Aquac Nutr 17(3):e741–e749. https://doi.org/10.1111/j.1365-2095.2010.00841.x

    Article  Google Scholar 

  30. Atencio L, Moreno I, Jos A, Prieto AI, Moyano R, Blanco A, Camean AM (2009) Effects of dietary selenium on the oxidative stress and pathological changes in tilapia (Oreochromis niloticus) exposed to a microcystin-producing cyanobacterial water bloom. Toxicon 53(2):269–282. https://doi.org/10.1016/j.toxicon.2008.11.011

    Article  CAS  PubMed  Google Scholar 

  31. De Riu N, Lee JW, Huang SS, Moniello G, Hung SS (2014) Effect of dietary selenomethionine on growth performance, tissue burden, and histopathology in green and white sturgeon. Aquat Toxicol 148:65–73. https://doi.org/10.1016/j.aquatox.2013.12.030

    Article  CAS  PubMed  Google Scholar 

  32. Zhang M, Xiao-Qian LU, Wang ZF, Yang S, Dang ZQ, Sang TC, Liu JB, Zhou W (2015) Accumulation of selenium in tissues of adult sea cucumber Apostichopus japonicus. Chin J Fish 28(5):18–22

    CAS  Google Scholar 

  33. Ciardullo S, Aureli F, Coni E, Guandalini E, Iosi F, Raggi A, Rufo G, Cubadda F (2008) Bioaccumulation potential of dietary arsenic, cadmium, lead, mercury, and selenium in organs and tissues of rainbow trout (Oncorhyncus mykiss) as a function of fish growth. J Agric Food Chem 56(7):2442–2451. https://doi.org/10.1021/jf703572t

    Article  CAS  PubMed  Google Scholar 

  34. Fontagné-Dicharry S, Véron V, Larroquet L, Godin S, Wischhusen P, Aguirre P, Terrier F, Richard N, Bueno M, Bouyssière B, Antony Jesu Prabhu P, Tacon P, Kaushik SJ (2020) Effect of selenium sources in plant-based diets on antioxidant status and oxidative stress-related parameters in rainbow trout juveniles under chronic stress exposure. Aquaculture 529:735684. https://doi.org/10.1016/j.aquaculture.2020.735684

    Article  CAS  Google Scholar 

  35. Rider SA, Davies SJ, Jha AN, Fisher AA, Knight J, Sweetman JW (2009) Supra-nutritional dietary intake of selenite and selenium yeast in normal and stressed rainbow trout (Oncorhynchus mykiss): Implications on selenium status and health responses. Aquaculture 295(3-4):282–291. https://doi.org/10.1016/j.aquaculture.2009.07.003

    Article  CAS  Google Scholar 

  36. KÜÇÜKBAY FZ, Yazlak H, Karaca I, Sahin N, Tuzcu M, Cakmak MN, Sahin K (2009) The effects of dietary organic or inorganic selenium in rainbow trout (Oncorhynchus mykiss) under crowding conditions. Aquac Nutr 15(6):569–576. https://doi.org/10.1111/j.1365-2095.2008.00624.x

    Article  CAS  Google Scholar 

  37. Lin YH, Shiau SY (2007) The effects of dietary selenium on the oxidative stress of grouper, Epinephelus malabaricus, fed high copper. Aquaculture 267(1-4):38–43. https://doi.org/10.1016/j.aquaculture.2006.12.015

    Article  CAS  Google Scholar 

  38. Penglase S, Hamre K, Rasinger JD, Ellingsen S (2014) Selenium status affects selenoprotein expression, reproduction, and F1 generation locomotor activity in zebrafish (Danio rerio). Br J Nutr 111(11):1918–1931. https://doi.org/10.1017/s000711451300439x

    Article  CAS  PubMed  Google Scholar 

  39. Fontagné-Dicharry S, Véron V, Larroquet L, Godin S, Kaushik SJ (2020) Effect of selenium sources in plant-based diets on antioxidant status and oxidative stress-related parameters in rainbow trout juveniles under chronic stress exposure. Aquaculture:735684. doi:https://doi.org/10.1016/j.aquaculture.2020.735684

  40. Del Rio AM, Davis BE, Fangue NA, Todgham AE (2019) Combined effects of warming and hypoxia on early life stage Chinook salmon physiology and development. Conserv Physiol 7(1):coy078. https://doi.org/10.1093/conphys/coy078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wang L, Xiao J-X, Hua Y, Xiang X-W, Zhou Y-F, Ye L, Shao Q-J (2019) Effects of dietary selenium polysaccharide on growth performance, oxidative stress and tissue selenium accumulation of juvenile black sea bream, Acanthopagrus schlegelii. Aquaculture 503:389–395. https://doi.org/10.1016/j.aquaculture.2019.01.033

    Article  CAS  Google Scholar 

  42. Levander OA (2000) The selenium-coxsackievirus connection: chronicle of a collaboration. J Nutr 130(2S Suppl):485S–488S. https://doi.org/10.1093/jn/130.2.485S

    Article  CAS  PubMed  Google Scholar 

  43. Hussein O, Rosenblat M, Refael G, Aviram M (1997) Dietary selenium increases cellular glutathione peroxidase activity and reduces the enhanced susceptibility to lipid peroxidation of plasma and low-density lipoprotein in kidney transplant recipients. Transplantation 63(5):679–685. https://doi.org/10.1097/00007890-199703150-00012

    Article  CAS  PubMed  Google Scholar 

  44. Prabhu KS, Nagaraja TP, Gandhi UH (2013) Selenoproteins and their role in oxidative stress and inflammation. Curr Chem Biol 7(1):65–73. https://doi.org/10.2174/2212796811307010007

    Article  Google Scholar 

  45. Wang J, Ren T, Han Y, Zhao Y, Liao M, Wang F, Jiang Z (2015) The effects of dietary lead on growth, bioaccumulation and antioxidant capacity in sea cucumber, Apostichopus japonicus. Environ Toxicol Pharmacol 40(2):535–540. https://doi.org/10.1016/j.etap.2015.08.012

    Article  CAS  PubMed  Google Scholar 

  46. Zhang Y, Meng D, Wang Z, Guo H, Wang Y (2012) Oxidative stress response in two representative bacteria exposed to atrazine. FEMS Microbiol Lett 334(2):95–101. https://doi.org/10.1111/j.1574-6968.2012.02625.x

    Article  CAS  PubMed  Google Scholar 

  47. Dotan Y, Lichtenberg D, Pinchuk I (2004) Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 43(3):200–227. https://doi.org/10.1016/j.plipres.2003.10.001

    Article  CAS  PubMed  Google Scholar 

  48. Chen H, Li J, Yan L, Cao J, Li D, Huang GY, Shi WJ, Dong W, Zha J, Ying GG, Zhong H, Wang Z, Huang Y, Luo Y, Xie L (2020) Subchronic effects of dietary selenium yeast and selenite on growth performance and the immune and antioxidant systems in Nile tilapia Oreochromis niloticus. Fish Shellfish Immunol 97:283–293. https://doi.org/10.1016/j.fsi.2019.12.053

    Article  CAS  PubMed  Google Scholar 

  49. Wang W, Mai K, Zhang W, Xu W, Ai Q, Liufu Z, Li H (2012) Dietary selenium requirement and its toxicity in juvenile abalone Haliotis discus hannai Ino. Aquaculture 330-333:42–46. https://doi.org/10.1016/j.aquaculture.2011.11.032

    Article  CAS  Google Scholar 

  50. Laparra JM, Sanz Y (2010) Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 61(3):219–225. https://doi.org/10.1016/j.phrs.2009.11.001

    Article  CAS  PubMed  Google Scholar 

  51. Zhu Y, Chen Y, Liu Y, Yang H, Liang G, Tian L (2012) Effect of dietary selenium level on growth performance, body composition and hepatic glutathione peroxidase activities of largemouth bass Micropterus salmoide. Aquac Res 43(11):1660–1668. https://doi.org/10.1111/j.1365-2109.2011.02972.x

    Article  CAS  Google Scholar 

  52. Bai Z, Ren T, Han Y, Rahman MM, Hu Y, Li Z, Jiang Z (2019) Influences of dietary selenomethionine exposure on tissue accumulation, blood biochemical profiles, gene expression and intestinal microbiota of Carassius auratus. Comp Biochem Physiol Toxicol Pharmacol 218:21–29. https://doi.org/10.1016/j.cbpc.2018.12.001

    Article  CAS  Google Scholar 

  53. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL (2010) Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 141(7):1241–1252. https://doi.org/10.1016/j.cell.2010.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Foster LH, Sumar S (2009) Selenium in health and disease: a review. Crit Rev Food Sci Nutr 37(3):211–228. https://doi.org/10.1080/10408399709527773

    Article  Google Scholar 

  55. Zhao Y, Liu H, Wang Q, Li B, Zhang H, Pi Y (2019) The effects of benzo[a]pyrene on the composition of gut microbiota and the gut health of the juvenile sea cucumber Apostichopus japonicus Selenka. Fish Shellfish Immunol 93:369–379. https://doi.org/10.1016/j.fsi.2019.07.073

    Article  CAS  PubMed  Google Scholar 

  56. Chen H, Li C, Liu T, Chen S, Xiao H (2019) A metagenomic study of intestinal microbial diversity in relation to feeding habits of surface and cave-dwelling Sinocyclocheilus species. Microb Ecol 79(2):299–311. https://doi.org/10.1007/s00248-019-01409-4

    Article  PubMed  Google Scholar 

  57. Gram L, Melchiorsen J, Spanggaard B, Huber I, Nielsen TF (1999) Inhibition of vibrio anguillarum by Pseudomonas fluorescens AH2, a possible probiotic treatment of fish. Appl Environ Microbiol 65(3):969–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Sharifah EN, Eguchi M (2012) Benefits of live phytoplankton, Chlorella vulgaris, as a biocontrol agent against fish pathogen Vibrio anguillarum. Fish Sci 78(2):367–373. https://doi.org/10.1007/s12562-011-0465-1

    Article  CAS  Google Scholar 

  59. Yang G, Xu Z, Tian X, Dong S, Peng M (2015) Intestinal microbiota and immune related genes in sea cucumber (Apostichopus japonicus) response to dietary beta-glucan supplementation. Biochem Biophys Res Commun 458(1):98–103. https://doi.org/10.1016/j.bbrc.2015.01.074

    Article  CAS  PubMed  Google Scholar 

  60. Yamazaki Y, Meirelles PM, Mino S, Suda W, Oshima K, Hattori M, Thompson FL, Sakai Y, Sawabe T, Sawabe T (2016) Individual Apostichopus japonicus fecal microbiome reveals a link with polyhydroxybutyrate producers in host growth gaps. Sci Rep 6:21631. https://doi.org/10.1038/srep21631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kasaikina MV, Kravtsova MA, Lee BC, Seravalli J, Peterson DA, Walter J, Legge R, Benson AK, Hatfield DL, Gladyshev VN (2011) Dietary selenium affects host selenoproteome expression by influencing the gut microbiota. FASEB J 25(7):2492–2499. https://doi.org/10.1096/fj.11-181990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the engineer Liu Yao at Public Technology Service Center, Institute of Oceanology, Chinese Academy of Sciences, for contribution in the determination of selenium content.

Funding

This work was supported by the National Key Research and Development Program of China (2018YFD0901103); the China Ocean Mineral Resources R&D Association (DY135-B2-14); Leading talent of Taishan Industry (tscy20190308); the Basic Scientific Fund for National Public Research Institutes of China (2020Q02); the Natural Science Foundation of Shandong (ZR2019BD023); the Key Research and Development Program of Shandong Province (2018GHY115034); and Ningbo Public Service Platform for High-Value Utilization of Marine Biological Resources (NBHY-2017-P2).

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Eco-Environmental Science and Technology, The First Institute of Oceanography, Ministry of Natural Resources, Qingdao, 266061, China

    Kai Wang, Yingying He, Changfeng Qu & Jinlai Miao

  2. Department of Specialty Medicine, School of Basic Medicine, Qingdao University, Qingdao, 266071, China

    Lina Liu & Jinlai Miao

  3. Laboratory for Marine Drugs and Bioproducts, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    Changfeng Qu & Jinlai Miao

Authors
  1. Kai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lina Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingying He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Changfeng Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinlai Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jinlai Miao.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, K., Liu, L., He, Y. et al. Effects of Dietary Supplementation with κ-Selenocarrageenan on the Selenium Accumulation and Intestinal Microbiota of the Sea Cucumbers Apostichopus japonicus. Biol Trace Elem Res 199, 2753–2763 (2021). https://doi.org/10.1007/s12011-020-02393-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02393-4

Keywords

Search

Navigation