Skip to main content
SpringerLink
Log in

Wheat grains fermented by fungal mycelia (Pleurotus ostreatus or Lentinus edodes) as alternative feed ingredients for juvenile rainbow trout (Oncorhynchus mykiss)

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

We investigated the effects of replacing non-fermented wheat grains with wheat grains fermented by fungal mycelia in the diet of juvenile rainbow trout (Oncorhynchus mykiss). We assessed growth performance, feeding parameters, and body composition in three experimental groups (0.33 ± 0.01 g, in triplicates of 50 individuals each). The diets for all the groups contained ca. 43% protein and 19% lipids. Experimental diets were made by replacing the 100 g kg−1 of wheat grains present in the basal diet (CTRL) with the same proportion of wheat grains fermented by Pleurotus ostreatus (PWD) or Lentinus edodes (LWD) mycelium. Fish were fed to apparent satiation twice a day for 56 days. Both, PWD and LWD, significantly increased fish body weight from day 28 onwards. Final body weight was 2.37 ± 0.04 g (CTRL), 4.29 ± 0.02 g (PWD), and 3.50 ± 0.05 g (LWD), and feeding efficiency (%) was increased from 64.5 ± 0.7 (CTRL) to 92.5 ± 0.5 (PWD) and 84.8 ± 1.5 (LWD). The experimental diets also improved nutrient retention efficiency (%): 30.0 ± 0.5 (PWD), 27.7 ± 1.1 (LWD), and 21.0 ± 0.1 (CTRL), for crude protein; 40.3 ± 0.6 (PWD), 31.0 ± 1.8 (LWD), and 16.1 ± 0.7 (CTRL), for ether extract; and 16.1 ± 0.1 (PWD), 14.0 ± 0.3 (LWD), and 11.6 ± 0.6 (CTRL), for phosphorus. Body lipid content was highest for PWD followed by LWD and CTRL (81.4 ± 1.4, 63.2 ± 2.5, 42.3 ± 2.6 g kg−1, respectively), while viscerosomatic index was lowest for PWD (p < 0.05). Liver glycogen in LWD and PWD fish (0.62 ± 0.10 and 0.21 ± 0.08% liver weight) was significantly higher than in CTRL fish (0.05 ± 0.01% liver weight). Wheat-mycelium meals appear to be suitable dietary ingredients for improving juvenile rainbow trout growth and nutritional performance. These benefits vary according to the mushroom species used.

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

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CP:

Crude protein

EE :

Ether extract

FBW:

Final body weight

FD:

Feed delivered

FE:

Feed efficiency

IBW:

Initial body weight

LAB :

Lactic acid bacteria

LW:

L. edodes wheat-mycelium meal

LWD:

L. edodes wheat-mycelium diet

P:

Phosphorus

PW:

P. ostreatus wheat-mycelium meal

PWD:

P. ostreatus wheat-mycelium diet

SSF :

Solid state fermentation

TGC:

Thermal growth coefficient

VSI :

Viscerosomatic index

WW :

Whole wheat grains

References

  • Ahmed M, Abdullah N, Shuib A et al (2015) Improvement of growth and antioxidant status in Nile tilapia, Oreochromis niloticus, fed diets supplemented with mushroom stalk waste hot water extract. Aquac Res 48:1146–1157

    Article  Google Scholar 

  • Aida F, Shuhaimi M et al (2009) Mushroom as a potential source of prebiotics: a review. Trends Food Sci Technol 20:567–575

    Article  CAS  Google Scholar 

  • AOAC (1990) Official methods of analysis of AOAC international, 15th edn. Association of official analytical chemists international, Arlington

    Google Scholar 

  • Baba E, Uluköy G, Önta C (2015) Effects of feed supplemented with Lentinula edodes mushroom extract on the immune response of rainbow trout, Oncorhynchus mykiss, and disease resistance against Lactococcus garvieae. Aquaculture 448:476–482

    Article  CAS  Google Scholar 

  • Barnes ME, Brown ML, Bruce T, Sindelar S, Neiger R (2014) Rainbow trout rearing performance, intestinal morphology, and immune response after long-term feeding of high levels of fermented soybean meal. N Am J Aquac 76:333–345

    Article  Google Scholar 

  • Bhanja Dey T, Kuhad RC (2014) Enhanced production and extraction of phenolic compounds from wheat by solid-state fermentation with Rhizopus oryzae RCK2012. Biotechnol Rep (Amst) 4:120–127

    Article  Google Scholar 

  • Bhanja Dey T, Kumari A, Banerjee R (2009) Enrichment of phenolics and free radical scavenging property of wheat koji prepared with two filamentous fungi. Bioresour Technol 100:2861–2866

    Article  Google Scholar 

  • Bilen S, Ünal S, Güvensoy H (2016) Effects of oyster mushroom (Pleurotus ostreatus) and nettle (Urtica dioica) methanolic extracts on immune responses and resistance to Aeromonas hydrophila in rainbow trout (Oncorhynchus mykiss). Aquaculture 454:90–94

    Article  Google Scholar 

  • Bisen PS, Baghel RK, Sanodiya BS, Thakur GS, Prasad GBKS (2010) Lentinus edodes: a macrofungus with pharmacological activities. Curr Med Chem 17:2419–2430

    Article  CAS  Google Scholar 

  • Boujard T, Leatherland JF (1992) Circadian pattern of hepatosomatic index, liver glycogen and lipid content, plasma non-esterified fatty acid, glucose, T3, T4, growth hormone and cortisol concentrations in Oncorhynchus mykiss held under different photoperiod regimes and fed using demand-feeders. Fish Physiol Biochem 10:111–122

    Article  CAS  Google Scholar 

  • Chang C, Huang SL, Chen S, Chen SN (2013) Innate immune responses and efficacy of using mushroom β-glucan mixture on orange-spotted grouper, Epinephelus coioides, aquaculture. Fish Shellfish Immunol 35:115–125

    Article  CAS  Google Scholar 

  • Cohen R, Persky L, Hadar Y (2002) Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Appl Microbiol Biotechnol 58:582–594

    Article  CAS  Google Scholar 

  • Cohen N, Cohen J, Asatiani MD, Varshney VK, Yu HT, Yang YC, Li YH, Mau JL, Wasser SP (2014) Chemical composition and nutritional and medicinal value of fruit bodies and submerged cultured mycelia of culinary-medicinal higher Basidiomycetes mushrooms. Int J Med Mushrooms 16:273–291

    Article  CAS  Google Scholar 

  • da Luz JMR, Paes SA, Torres DP et al (2013) Production of edible mushroom and degradation of antinutritional factors in Jatropha biodiesel residues. Food Sci Technol 50:575–580

    Google Scholar 

  • Deepalakshmi K, Mirunalini S (2014) Pleurotus ostreatus: an oyster mushroom with nutritional and medicinal properties. J Biochem Tech 5:718–726

    Google Scholar 

  • Djordjevic B, Skugor S, Jørgensen SM et al (2009) Modulation of splenic immune responses to bacterial lipopolysaccharide in rainbow trout (Oncorhynchus mykiss) fed lentinan, a β-glucan from mushroom Lentinula edodes. Fish Shellfish Immunol 26:201–209

    Article  CAS  Google Scholar 

  • Dobsíková R, Blahová J, Mikulíková I et al (2013) The effect of oyster mushroom β-1.3/1.6-D-glucan and oxytetracycline antibiotic on biometrical, haematological, biochemical, and immunological indices, and histopathological changes in common carp (Cyprinus carpio L). Fish Shellfish Immunol 35:1813–1823

    Article  Google Scholar 

  • dos Santos MM, Souza da Rosa AS et al (2004) Thermal denaturation: is solid-state fermentation really a good technology for the production of enzymes? Bioresour Technol 93:261–268

    Article  Google Scholar 

  • Dumas A, France J, Bureau DP (2007) Evidence of three growth stanzas in rainbow trout (Oncorhynchus mykiss) across life stages and adaptation of the thermal-unit growth coefficient. Aquaculture 267:139–146

    Article  Google Scholar 

  • Gan R, Li H, Gunaratne A et al (2017) Effects of fermented edible seeds and their products on human health: bioactive components and bioactivities. Compr Rev Food Sci Food Saf 16:489–531

    Article  CAS  Google Scholar 

  • Gilmour KM, Kirkpatrick S, Massarsky A, Pearce B, Saliba S, Stephany CÉ, Moon TW (2012) The influence of social status on hepatic glucose metabolism in rainbow trout Oncorhynchus mykiss. Physiol Biochem Zool 85:309–320

    Article  CAS  Google Scholar 

  • Glencross B, Hawkins W, Curnow J (2004) Nutritional assessment of Australian canola meals. II. Evaluation of the influence of the canola oil extraction method on the protein value of canola meals fed to the red seabream (Pagrus auratus, Paulin). Aquac Res 35:25–34

    Article  CAS  Google Scholar 

  • Glencross B, Booth M, Allan GL (2007) A feed is only as good as its ingredients – a review of ingredient evaluation strategies for aquaculture feeds. Aquac Nutr 13:17–34

    Article  CAS  Google Scholar 

  • Gowthaman NK, Chundakkadu K, Moo-Young M (2001) Fungal solid state fermentation – an overview. In: Khachatourians GG, Arora DK (eds) Applied mycology and biotechnology for agriculture and foods. Elsevier, vol 1, pp1–11

  • Hardy R (2002) Rainbow trout Oncorhynchus mykiss. In: Webster CD, Lim CE (eds) Nutrient requirements and feeding of finfish for aquaculture. CABI Publishing, New York, pp 184–202

    Chapter  Google Scholar 

  • Hearst R, Nelson D, McCollum G, Millar BC, Maeda Y, Goldsmith CE, Rooney PJ, Loughrey A, Rao JR, Moore JE (2009) An examination of antibacterial and antifungal properties of constituents of shiitake (Lentinula edodes) and oyster (Pleurotus ostreatus) mushrooms. Complement Ther Clin Pract 15:5–7

    Article  Google Scholar 

  • Hemre EI, Mommsen TP, Krogdahl A (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

    Article  CAS  Google Scholar 

  • Hilton JW, Dixon DG (1982) Effect of increased liver glycogen and liver weight on liver function in rainbow trout, Salmo gairdneri Richardson: recovery from anaesthesia and plasma 35S-sulphobromophthalein clearance. J Fish Dis 5:185–195

    Article  CAS  Google Scholar 

  • Hilton JW, Slinger SJ (1981) Nutrition and feeding of rainbow trout. Can Spec Publ Fish Aquat Sci 55:15 p

  • Hole AS, Rud I, Grimmer S, Sigl S, Narvhus J, Sahlstrøm S (2012) Improved bioavailability of dietary phenolic acids in whole grain barley and oat groat following fermentation with probiotic Lactobacillus acidophilus, Lactobacillus johnsonii, and Lactobacillus reuteri. J Agric Food Chem 60:6369–6375

    Article  CAS  Google Scholar 

  • Kamilya D, Ghosh D, Bandyopadhayay S et al (2006) In vitro effects of bovine lactoferrin, mushroom glucan and Abrus agglutinin on Indian major carp, catla (Catla catla) head kidney leukocytes. Aquaculture 253:130–139

    Article  CAS  Google Scholar 

  • Katya K, Yun Y, Park G, Lee JY, Yoo G, Bai SC (2014) Evaluation of the efficacy of fermented by-product of mushroom, Pleurotus ostreatus, as a fish meal replacer in juvenile amur catfish: effects on growth, serological characteristics and immune responses. Asian Australas J Anim Sci 27:1478–1486

    Article  CAS  Google Scholar 

  • Kause A, Kiessling A, Martin SA (2016) Genetic improvement of feed conversion ratio via indirect selection against lipid deposition in farmed rainbow trout (Oncorhynchus mykiss Walbaum). Br J Nutr 116:1656–1665

    Article  CAS  Google Scholar 

  • Kim JD, Kaushik SI (1992) Contribution of digestible energy from carbohydrates and estimation of protein requirements for growth of rainbow trout (Oncorhynchus mykiss). Aquaculure 106:161–169

    Article  Google Scholar 

  • Liu Y, Du J, Cao L et al (2015) Anti-inflammatory and hepatoprotective effect of Ganoderma lucidum polysaccharides on carbon tetrachloride-induced hepatocyte damage in common carp (Cyprinus carpio). Int Immunopharmacol 25:112–120

    Article  CAS  Google Scholar 

  • Lobanok AG, Babitskaya VG, Plenina LV, Puchkova TA, Osadchaya OV (2003) Composition and biological activity of submerged mycelium of the xylotrophic basidiomycete Lentinus edodes. Appl Biochem Microbiol 39:60–64

    Article  CAS  Google Scholar 

  • Merrill AL, Watt BK (1973) Energy value of foods: basis and derivation. Agriculture handbook No. 74. ARS United States Department of Agriculture, Washington DC

    Google Scholar 

  • Nasehi M, Torbatinejad NM, Zerehdaran S, Safaie AR (2017) Effect of solid-state fermentation by oyster mushroom (Pleurotus florida) on nutritive value of some agro by-products. J Appl Anim Res 45:221–226

    Article  CAS  Google Scholar 

  • Nikl L, Albright LJ, Evelyn T (1991) Influence of seven immunostimulants on the immune response of Coho salmon to Aeromonas salmonicida. Dis Aquat Org 12:7–12

    Article  CAS  Google Scholar 

  • Nout MJR, Kiers JL (2005) Tempe fermentation, innovation and functionality: update into the third millennium. J Appl Microbiol 98:789–805

    Article  CAS  Google Scholar 

  • NRC (National Research Council) (1993) Nutrient requirements of fish. The National Academies Press, Washington DC

    Google Scholar 

  • Pandey A (1992) Recent process developments in solid-state fermentation. Process Biochem 27:109–117

    Article  CAS  Google Scholar 

  • Pascual MM, Hualde JP, Bianchi VA, Castro JM, Luquet CM (2017) Diet supplemented with Grifola gargal mushroom enhances growth, lipid content, and nutrient retention of juvenile rainbow trout (Oncorhynchus mykiss). Aquac Int 25:1787–1797

    Article  CAS  Google Scholar 

  • Postemsky PD, Curvetto NR (2014) Enhancement of wheat grain antioxidant activity by solid state fermentation with Grifola spp. J Med Food 17:543–549

    Article  CAS  Google Scholar 

  • Reis FS, Barros L, Martins A, Ferreira ICFR (2012) Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: an inter-species comparative study. Food Chem Toxicol 50:191–197

    Article  CAS  Google Scholar 

  • Rodríguez Couto S, Sanromán MA (2006) Application of solid-state fermentation to food industry—a review. J Food Eng 76:291–302

    Article  Google Scholar 

  • Sandhu KS, Punia S, Kaur M (2016) Effect of duration of solid state fermentation by Aspergillus awamorinakazawa on antioxidant properties of wheat cultivars. Food Sci Technol 71:323–328

    CAS  Google Scholar 

  • Schneider I, Kressel G, Meyer A et al (2011) Lipid lowering effects of oyster mushroom (Pleurotus ostreatus) in humans. J Funct Foods 3:17–24

    Article  CAS  Google Scholar 

  • Singh nee’ Nigam P, Pandey A (2009) Solid-state fermentation technology for bioconversion of biomass and agricultural residues. In: Singh nee’ Nigam P, Pandey A (eds) Biotechnology for agro-industrial residues utilisation. Springer, Dordrecht

    Chapter  Google Scholar 

  • Singhania R, Patel A, Soccol C et al (2009) Recent advances in solid-state fermentation. Biochem Eng J 44:13–18

    Article  CAS  Google Scholar 

  • Skrede G, Storebakken T, Skrede A (2002) Lactic acid fermentation of wheat and barley whole meal flours improves digestibility of nutrients and energy in Atlantic salmon (Salmo salar L.) diets. Aquaculture 210:305–321

    Article  CAS  Google Scholar 

  • Steinkraus KH (1994) Nutritional significance of fermented food. Food Res Int 27:259–267

    Article  Google Scholar 

  • Subramaniam S, Sabaratnam V, Kuppusamy UR, Tan YS (2014) Solid-substrate fermentation of wheat grains by mycelia of indigenous species of the genus Ganoderma (higher Basidiomycetes) to enhance the antioxidant activities. Int J Med Mushrooms 16:259–267

    Article  CAS  Google Scholar 

  • Takeuchi T (1988) Laboratory work chemical evaluation of dietary nutrients. In: Watanabe T (ed) Fish nutrition and mariculture. JICA Textbook the General Aquaculture Course, Tokyo, pp 198–199

    Google Scholar 

  • Thomas L, Larroche C, Pandey A (2013) Current development in solid-state fermentation. Biochem Eng J 81:146–161

    Article  CAS  Google Scholar 

  • Uluköy G, Baba E, Birincioğlu S (2016) Effects of dietary Lentinula edodes extract on liver and gut histology of rainbow trout (Oncorhynchus mykiss, Walbaum 1792). Fish Shellfish Immunol 53:106

    Article  Google Scholar 

  • Van Doan H, Doolgindachbaporn S, Suksri A (2016) Effects of Eryngii mushroom (Pleurotus eryngii) and Lactobacillus plantarum on growth performance, immunity and disease resistance of Pangasius catfish (Pangasius bocourti, Sauvage 1880). Fish Physiol Biochem 42:1427–1440

    Article  Google Scholar 

  • Van Handel E (1965) Estimation of glycogen in small amounts of tissue. Anal Biochem 11:256–265

    Article  Google Scholar 

  • Wani BA, Bodha RH, Wani AH (2010) Nutritional and medicinal importance of mushrooms. J Med Plant Res 4:2598–2604

    Article  Google Scholar 

  • Wasser SP (2014) Medicinal mushroom science: current perspectives, advances, evidences, and challenges. Biom J 37:354–356

    Google Scholar 

  • Woynarovich A, Hoitsy G, Moth-Poulsen T (2011) Small-scale rainbow trout farming. FAO Fisheries and Aquaculture Technical Paper No. 561. Food and Agriculture Organization of the United Nations, Rome, p 81

  • Yin G, Ardó L, Thompson KD, Adams A, Jeney Z, Jeney G (2009) Chinese herbs (Astragalus radix and Ganoderma lucidum) enhance immune response of carp Cyprinus carpio, and protection against Aeromonas hydrophila. Fish Shellfish Immunol 26:140–145

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Zhang Z, Lv G, Pan H et al (2012) Production of powerful antioxidant supplements via solid-state fermentation of wheat (Triticum aestivum Linn.) by Cordyceps militaris. Food Technol Biotechnol 50:32–39

    Google Scholar 

Download references

Acknowledgements

The authors wish to thank Pablo Morzenti and Antonio Miloro for their contributions to this work. We acknowledge the helpful suggestions of two anonymous reviewers.

Funding

This study was supported by the grants CONICET PIP 11220130100529 and ANPCYT PICT 2013-1415 to CML. This study also received funding from Ministerio de Seguridad and Trabajo y Ambiente de la Provincia de Neuquén.

Author information

Authors and Affiliations

  1. Laboratorio de Ecotoxicología Acuática, INIBIOMA (CONICET-UNCo) – CEAN, ruta provincial no. 61, km 3, CCP 7, Junín de los Andes, 8371, Neuquén, Argentina

    Mariano M. Pascual, Virginia A. Bianchi, Juan M. Castro & Carlos M. Luquet

  2. Centro de Ecología Aplicada del Neuquén (CEAN), Junín de los Andes, Neuquén, Argentina

    Juan P. Hualde & Pablo Moreno

Authors
  1. Mariano M. Pascual
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan P. Hualde
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Virginia A. Bianchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juan M. Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carlos M. Luquet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mariano M. Pascual.

Ethics declarations

The experimental protocols were approved by the Bioethics Committee, School of Biochemical and Pharmaceutical Sciences, National University of Rosario, Argentina (6060/116).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pascual, M.M., Hualde, J.P., Bianchi, V.A. et al. Wheat grains fermented by fungal mycelia (Pleurotus ostreatus or Lentinus edodes) as alternative feed ingredients for juvenile rainbow trout (Oncorhynchus mykiss). Aquacult Int 26, 1339–1352 (2018). https://doi.org/10.1007/s10499-018-0286-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-018-0286-7

Keywords

Search

Navigation