Skip to main content
SpringerLink
Log in

Iron Bioaccumulation in Lentinus crinitus Mycelia Cultivated in Agroindustrial Byproducts

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Iron deficiency anemia is a challenge to global public health, and the development of iron-enriched foods are an opportunity to reduce this problem. Lentinus crinitus is a basidiomycete with high metal bioaccumulation capacity that is consumed by Amazonian Indians. This study aimed to evaluate iron bioaccumulation in the mycelial biomass of L. crinitus cultivated in agroindustrial byproducts. First, the fungus grew in a liquid medium with iron addition from 0.116 (control) to 100 mg L−1. The addition of 90 mg L−1 iron to the culture medium resulted in 15.07 ± 1.44 dg kg−1 of iron mycelial bioaccumulation, a 9000-fold increase compared with the control. Then, the fungus grew in agroindustrial byproducts sugarcane (SCM) or soybean (SBM) molasses added with 90 mg L−1 iron and 0.9 mg L−1 manganese, a new element in the assay. The iron concentrations in the mycelial biomass cultivated in SCM or SBM were 20.78 ± 2.28 or 34.71 ± 4.31 dg kg−1, respectively, at 21 cultivation days. The cultivation time and the presence of iron and manganese in the culture media were important variables for iron bioaccumulation in the mycelial biomass. Our study evidenced that agroindustrial byproducts, mainly SCM, can be used to successfully produce mycelial biomass enriched with iron - as an alternative functional food - to add value to the food production chain. Also, the iron-enriched biomass can be an alternative for non-living animal protein supply.

Graphical abstract

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Shubham, K., Anukiruthika, T., Dutta, S., Kashyap, A.V., Moses, J.A., Anandharamakrishnan, C.: Iron deficiency anemia: a comprehensive review on iron absorption, bioavailability and emerging food fortification approaches. Trends Food Sci. Technol. 99, 58–75 (2020). https://doi.org/10.1016/j.tifs.2020.02.021

    Article  Google Scholar 

  2. Lopez, A., Cacoub, P., Macdougall, I.C., Peyrin-Biroulet, L.: Iron deficiency anaemia. Lancet. 387, 907–916 (2016). https://doi.org/10.1016/S0140-6736(15)60865-0

    Article  Google Scholar 

  3. WHO – World Health Organization: The global prevalence of anemia in 2011. WHO, Geneva. https://apps.who.int/iris/bitstream/handle/10665/177094/9789241564960_eng.pdf?sequence=1 (2015) Accessed 10 Mar 2020

  4. WHO – World Health Organization, Department of Nutrition for Health and Development. Global nutrition targets 2025: anemia policy brief. WHO/NMH/NHD, Geneve. file:///C:/Users/Usuario/Downloads/WHO_NMH_NHD_14.4_eng.pdf. (2014). Accessed 10 Mar 2020

  5. Manoguerra, A.S., Erdman, A.R., Booze, L.L., Christianson, G., Wax, P.M., Scharman, E.J., Woolf, A.D., Chyka, P.A., Keyes, D.C., Olson, K.R., Caravati, E.M., Troutman, W.G.: Iron ingestion: an evidence-based consensus guideline for out-of-hospital management. Clin. Toxicol. 43, 553–570 (2005). https://doi.org/10.1081/CLT-200068842

    Article  Google Scholar 

  6. Murray-Kolb, L.E., Beard, J.L.: In: Coates, P.M., Betz, J.M. (eds.) Encyclopedia of Dietary Supplements, pp. 432–438. London/New York, Informa Healthcare (2010)

    Chapter  Google Scholar 

  7. IOM – Institute of Medicine. Dietary Reference Intakes: the essential guide to nutrient requirements. National Academic, Washington DC: The National Academies Press. https://doi.org/10.17226/11537 (2006). Accessed 23 Feb 2020

  8. Mshandete, A.M., Mgonia, J.R.: Submerged liquid fermentation of some Tanzanian Basidiomycetes for the production of mycelial biomass, exopolysaccharides and mycelium protein using waste peel media. ARPN J. Agric. Biol. Sci. 4, 1–13 (2009)

    Article  Google Scholar 

  9. Almeida, S.M., Umeo, S.H., Marcante, R.C., Yokota, M.E., Valle, J.S., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Iron bioaccumulation in mycelium of Pleurotus ostreatus. Brazilian J. Microbiol. 46, 195–200 (2015). https://doi.org/10.1590/S1517-838246120130695

    Article  Google Scholar 

  10. Meniqueti, A.B., Ruiz, S.P., Faria, M.G.I., Valle, J.S., Gonçalves Jr., A.C., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Iron-enriched mycelia of edible and medicinal basidiomycetes. Environ. Technol. (2020). https://doi.org/10.1080/09593330.2020.1824023

  11. Umeo, S.H., Faria, M.G.I., Vilande, S.S.S., Dragunski, D.C., Do Valle, J.S., Colauto, N.B., Linde, G.A.: Iron and zinc mycelial bioaccumulation in Agaricus subrufescens strains. Semin. Agrar. 40, 2513–2522 (2019). https://doi.org/10.5433/1679-0359.2019v40n6p2513

    Article  Google Scholar 

  12. Faria, M.G.I., Do Valle, J.S., Lopes, A.D., Gonçalves, A.C., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Bioaccumulation of lithium (Li2CO3) in mycelia of the culinary-medicinal oyster mushroom, Pleurotus ostreatus (agaricomycetes). Int. J. Med. Mushrooms. 20, 901–907 (2018). https://doi.org/10.1615/IntJMedMushrooms.2018027343

    Article  Google Scholar 

  13. Marcante, R.D.C., Meniquetti, A., Pascotto, C.R., Gazim, Z.C., Magalhães, H.M., Colauto, N.B., Linde, G.A.: Bioacumulação de zinco em micélio de Agaricus subrufescens. Arq. Ciên. Vet. Zool. UNIPAR. 17, 249–252 (2015). https://doi.org/10.25110/arqvet.v17i4.2014.5025

    Article  Google Scholar 

  14. Silva, G.T., Gibertoni, T.B.: Aphyllophorales (Basidiomycota) em áreas urbanas da Região Metropolitana do Recife, PE. Brasil. Hoehnea. 33, 533–543 (2006)

    Google Scholar 

  15. Vargas-isla, R., Ishikawa, N.K., Py-daniel, V.: Contribuições etnomicológicas dos povos indígenas da Amazônia. Biota Amazônia. 3, 58–65 (2013)

    Article  Google Scholar 

  16. Abraham, W.R., Abate, D.: Antimicrobial metabolites from Lentinus crinitus. J. Antibiot. 47, 1348–1350 (1994). https://doi.org/10.7164/antibiotics.47.1348

    Article  Google Scholar 

  17. Tavares, M.F., Avelino, K.V., Araújo, N.L., Marim, R.A., Linde, G.A., Colauto, N.B., do Valle, J.S.: Decolorization of azo and anthraquinone dyes by crude laccase produced by Lentinus crinitus in solid state cultivation. Brazilian J. Microbiol. 51, 99–106 (2020). https://doi.org/10.1007/s42770-019-00189-w

    Article  Google Scholar 

  18. Caroline, E., Brito, D.M., Rodrigo, I., Braga, S., Francisca, M., Teixeira, S., Salomão, I.I., Martim, R.: Production and partial characterization of aspartic proteases synthesized by Lentinus crinitus (L.) Fr. 1825 DPUA 1693 (Polyporaceae). Bol. Mus. Para. Emílio Goeldi. Cienc. Nat. 14, 463–472 (2019)

    Google Scholar 

  19. Faria, M.G.I., Avelino, K.V., do Valle, J.S., da Silva, G.J., Gonçalves, A.C., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Lithium bioaccumulation in Lentinus crinitus mycelial biomass as a potential functional food. Chemosphere. 235, 538–542 (2019). https://doi.org/10.1016/j.chemosphere.2019.06.218

    Article  Google Scholar 

  20. Scheid, S.C., Faria, M.G.I., Velasquez, L.G., Valle, J.S., Gonçalves Jr., A.C., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Iron biofortification and availability in the mycelial biomass of edible and medicinal basidiomycetes cultivated in sugarcane molasses. Sci. Rep. 10, 12875 (2020). https://doi.org/10.1038/s41598-020-69699-0

    Article  Google Scholar 

  21. Umeo, S.H., Souza, G.P.N., Rapachi, P.M., Garcia, D.M., Paccola-Meirelles, L.D., Valle, J.S., Colauto, N.B., Linde, G.A.: Screening of basidiomycetes in submerged cultivation based on antioxidant activity. Genet. Mol. Res. 14, 9907–9914 (2015). https://doi.org/10.4238/2015.August.19.25

    Article  Google Scholar 

  22. Ravindran, R., Hassan, S.S., Williams, G.A., Jaiswal, A.K.: A review on bioconversion of agro-industrial wastes to industrially important enzymes. Bioengineering. 5, 1–20 (2018). https://doi.org/10.3390/bioengineering5040093

    Article  Google Scholar 

  23. Sadh, P.K., Duhan, S., Duhan, J.S.: Agro-industrial wastes and their utilization using solid state fermentation: a review. Bioresour. Bioprocess. 5, 1–15 (2018). https://doi.org/10.1186/s40643-017-0187-z

    Article  Google Scholar 

  24. CONAB - Companhia Nacional de Abastecimento. 2019. Acompanhamento da safra brasileira de cana-de-açúcar. CONAB, Brasília. Available at: https://www.conab.gov.br/info-agro/safras/cana/boletim-da-safra-de-cana-de-acucar (2019) Accessed 10 Feb 2020

  25. CONAB - Companhia Nacional de Abastecimento. 2019. Acompanhamento da safra brasileira de grãos. Available at: https://www.conab.gov.br/info-agro/safras/graos/boletim-da-safra-de-graos (2019) Accessed 10 Feb 2020

  26. Rein, P.: Cane Sugar Engineering, 768 p. VERLAG, Berlin (2007)

    Google Scholar 

  27. Dong, J., Du, Y., Zhou, Y., Yang, S.T.: Butanol production from soybean hull and soy molasses by acetone-butanol-ethanol fermentation. ACS Symp. Ser. 1178, 25–41 (2014). https://doi.org/10.1021/bk-2014-1178.ch002

    Article  Google Scholar 

  28. Siqueira, P.F., Karp, S.G., Carvalho, J.C., Sturm, W., Rodríguez-León, J.A., Tholozan, J.L., Singhania, R.R., Pandey, A., Soccol, C.R.: Production of bio-ethanol from soybean molasses by Saccharomyces cerevisiae at laboratory, pilot and industrial scales. Bioresour. Technol. 99, 8156–8163 (2008). https://doi.org/10.1016/j.biortech.2008.03.037

    Article  Google Scholar 

  29. De Pretto, C., de Giordano, R., Tardioli, P.W., Costa, C.B.B.: Possibilities for producing energy, fuels, and chemicals from soybean: a biorefinery concept. Waste Biomass Valorization. 9, 1703–1730 (2018). https://doi.org/10.1007/s12649-017-9956-3

    Article  Google Scholar 

  30. Philpott, C.C.: Iron uptake in fungi: a system for every source. Biochim. Biophys. Acta, Mol. Cell Res. 1763, 636–645 (2006). https://doi.org/10.1016/j.bbamcr.2006.05.008

    Article  Google Scholar 

  31. Ines, M., Amel, K., Yousra, T., Neila, S., Imen, D., Marie, M.J., Abdennasseur, H.: Effect of dose-response of zinc and manganese on siderophores production. Am. J. Environ. Sci. 8, 143–151 (2012). https://doi.org/10.3844/ajessp.2012.143.151

    Article  Google Scholar 

  32. Zaghi Jr., L.L.Z., Lopes, A.D., Cordeiro, F.A., Colla, I.M., Bertéli, M.B.D., Valle, J.S., do Linde, G.A., Colauto, N.B.: Cryopreservation at −75 °C of Agaricus subrufescens on wheat grains with sucrose. Brazilian J. Microbiol. 49, 370–377 (2018). https://doi.org/10.1016/j.bjm.2017.08.003

    Article  Google Scholar 

  33. Ciabotti, S.: Aspectos químico, físico-químico e sensorial de extratos de soja e tofus obtidos dos cultivares de soja convencional e livre de lipoxigenase. Dissertação (Mestrado em Ciência de Alimentos) - Universidade Federal de Minas Gerais. 135 (2004)

  34. AOAC - Official Methods of Analysis. Association of Official Analytical Chemists, 15th ed, Vol 2, Inc, Washington DC, 1990

  35. Kosman, D.J.: Molecular mechanisms of iron uptake in fungi. Mol. Microbiol. 47, 1185–1197 (2003). https://doi.org/10.1046/j.1365-2958.2003.03368.x

    Article  Google Scholar 

  36. Gadd, G.M.: Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 111, 3–49 (2007). https://doi.org/10.1016/j.mycres.2006.12.001

    Article  Google Scholar 

  37. Ogidi, O.C., Nunes, M.D., Oyetayo, V.O., Akinyele, B.J., Kasuya, M.C.M.: Mycelial growth, biomass production and Iron uptake by mushrooms of Pleurotus species cultivated on Urochloa decumbens (Stapf) R. D. Webster. J. Food Res. 5, 13 (2016). https://doi.org/10.5539/jfr.v5n3p13

    Article  Google Scholar 

  38. Mleczek, M., Siwulski, M., Budka, A., Mleczek, P., Budzyńska, S., Szostek, M., Kuczyńska-Kippen, N., Kalač, P., Niedzielski, P., Gąsecka, M., Goliński, P., Magdziak, Z., RzymskI, P.: Toxicological risks and nutritional value of wild edible mushroom species -a half-century monitoring study. Chemosphere. 263, 128095 (2021). https://doi.org/10.1016/j.chemosphere.2020.128095

    Article  Google Scholar 

  39. Saha, R., Saha, N., Donofrio, R.S., Bestervelt, L.L.: Microbial siderophores: a mini review. J. Basic Microbiol. 53, 303–317 (2013). https://doi.org/10.1002/jobm.201100552

    Article  Google Scholar 

  40. Protchenko, O., Ferea, T., Rashford, J., Tiedeman, J., Brown, P.O., Botstein, D., Philpott, C.C.: Three Cell Wall Mannoproteins facilitate the uptake of Iron in Saccharomyces cerevisiae. J. Biol. Chem. 276, 49244–49250 (2001). https://doi.org/10.1074/jbc.M109220200

    Article  Google Scholar 

  41. Comensoli, L., Bindschedler, S., Junier, P., Joseph, E.: Iron and fungal physiology: a review of biotechnological opportunities. Elsevier Ltd. (2017)

  42. Braud, A., Hannauer, M., Mislin, G.L.A., Schalk, I.J.: The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J. Bacteriol. 191, 3517–3525 (2009). https://doi.org/10.1128/JB.00010-09

    Article  Google Scholar 

  43. Damodaran, D., Vidya Shetty, K., Raj Mohan, B.: Uptake of certain heavy metals from contaminated soil by mushroom-Galerina vittiformis. Ecotoxicol. Environ. Saf. 104, 414–422 (2014). https://doi.org/10.1016/j.ecoenv.2013.10.033

    Article  Google Scholar 

  44. Yokota, M.E., Frison, P.S., Marcante, R.C., Jorge, L.F., Valle, J.S., Dragunski, D.C., Colauto, N.B., Linde, G.A.: Iron translocation in Pleurotus ostreatus basidiocarps: production, bioavailability, and antioxidant activity. Genet. Mol. Res. 15, 1–10 (2016). https://doi.org/10.4238/gmr.15017888

    Article  Google Scholar 

  45. Ben-Arye, T., Levenberg, S.: Tissue engineering for clean meat production. Front. Sustain. Food Syst. 3, 46 (2019). https://doi.org/10.3389/fsufs.2019.00046

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Paranaense University, West Paraná State University, Fundação Araucária, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES).

Funding

This study was funded by Paranaense University, Fundação Araucária, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) -finance code 001- for the financial support and scholarships.

Author information

Authors and Affiliations

  1. Paranaense University, Graduate Program in Biotechnology Applied to Agriculture, Umuarama, Paraná, Brazil

    Adriano Borges Meniqueti, Suelen Pereira Ruiz, Maria Graciela Iecher Faria, Juliana Silveira do Valle, Nelson Barros Colauto & Giani Andrea Linde

  2. West Paraná State University, Laboratory of Environmental Chemistry, Center of Agricultural Science, Marechal Cândido Rondon, PR, Brazil

    Affonso Celso Gonçalves Jr.

  3. West Paraná State University, Center of Engineering and Exact Sciences, Toledo, PR, Brazil

    Douglas Cardoso Dragunski

Authors
  1. Adriano Borges Meniqueti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Suelen Pereira Ruiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Graciela Iecher Faria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juliana Silveira do Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Affonso Celso Gonçalves Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Douglas Cardoso Dragunski
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nelson Barros Colauto
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giani Andrea Linde
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ABM: Execution, analysis, investigation, writing of the draft. SPR: writing: reviewing and editing. MGIF: validation, writing: reviewing and editing. JSdV: conceptualization, validation, writing: reviewing and editing. ACGJr.: analysis, writing, critical reviewing, and editing. DCD: analysis, writing, critical reviewing, and editing. NBC: project administration, supervision, conceptualization, final writing: reviewing and editing. GAL: project administration, supervision, conceptualization, writing: critical reviewing and editing.

Corresponding author

Correspondence to Suelen Pereira Ruiz.

Ethics declarations

Conflict of interest

The authors declare that there are no 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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meniqueti, A.B., Ruiz, S.P., Faria, M.G.I. et al. Iron Bioaccumulation in Lentinus crinitus Mycelia Cultivated in Agroindustrial Byproducts. Waste Biomass Valor 12, 4965–4974 (2021). https://doi.org/10.1007/s12649-021-01353-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-021-01353-w

Keywords

Search

Navigation