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Potential of Cultivated Ganoderma lucidum

Mushrooms for the Production of Supplements

Enriched with Essential ElementsPiotr Rzymski, Mirosaw Mleczek, Przemysaw Niedzielski, Marek Siwulski, and Monika a!secka

"#stract$ Ganoderma lucidumis an important medicinal mushroom species and there is continuous interest in its bioactiveproperties. This study evaluated whether it may additionally serve as a nutritional supplement for the trace elements:selenium (Se), copper (Cu), and zinc (Zn). ushrooms were cultivated on substrates enriched with !." to !.# m ofinor$anic Se alone or in combination with Zn and%or Cu. Supplementation increased accumulation of the ele&ments infruitin$ bodies re$ardless of the applied cultivation model. G. lucidumdemonstrated the ability to accumulate si$ni'cantamounts of or$anic Se, maimally amountin$ to (i) over m$%*$ when the substrate was supplemented only with Se, (ii)over +! m$%*$ in the Se+Cu model, (iii) over + m$%*$ in the Se +Zn model, and (iv) " m$%*$ in the Se+Cu+Zn model.The accumulation of Cu and Zn steadily increased with their initial substrate concentra&tions. aimum concentrationsfound after supplementation with !.# m amounted to over m$%*$ (Se+Zn) and + m$%*$ (Se+Cu+Zn) of Zn, and +-m$%*$ (Se+Cu) and over " m$%*$ (Se+Cu+Zn) of Cu. The $reater the supplemented concentration and number ofsupplemented elements, the lower the biomass of G. lucidumfruitin$ bodies. /evertheless, it still remained hi$h when thesubstrate was supplemented up to !. m with each element. These results hi$hli$ht that G. lucidumcan easily incorporate

elements from the substrate and that, when bioforti'ed, its dried fruitin$ bodies may serve as a nutritional source of theseessential elements.

%eywords$ copper,Ganoderma lucidum, medicinal mushroom, selenium, zinc

Practical "pplication$ TheGanoderma lucidumfruitin$ bodies bioforti'ed with essential elements, such as Se, Cu, and Znin this study may have potential value for both nutritional and medicinal use. 0s shown, cultivation of this mushroomspecies with substrates enriched with Se, Se and Cu, Se and Zn or Se, Cu and Zn is uncomplicated, inepensive, and leadsto the production of relatively hi$h biomass of fruitin$ bodies. Considerin$ the popularity of G. lucidum, its bioforti'cationwith Se, Cu, and Zn may be of commercial interest.

C$&oodCh

emistry

'ntroduction1or centuries mushrooms have been collected for consumption

and health bene'ts, the latter ori$inatin$ mainly from traditionaleastern medicine (1erreira and others +!"!). /owadays, $lobalinterest in the pharmaceutical and dietary use of cultivated mush&rooms is on the rise. This is lar$ely due to an increasin$ number ofstudies providin$ convincin$ evidence of their nutritional andtherapeutic value, but also as a result of the commercialization ofautomated and relatively inepensive methods of mushroom cul&tivation (2alverde and others +!"). 3nli*e collected mushrooms,in which accumulation of toic substances in edible parts cannot becontrolled (4alac5 +!"6 lecze* and others +!"a), cultivationcan ensure supervised and hi$h&7uality conditions enablin$ the

'nal product to be standardized and safe for consumers (Chan$ and8asser +!"+6 Cleaver and others +!"+).

/utritional de'ciencies are a worldwide problem, they not onlylead to the development of serious health disorders, but also $ener&

MS 20151668 Submitted 10/7/2015, Accepted 12/12/2015. Author R!m"# i" $ith

%ept. o& 'n(ironmental Medicine, )onan *ni(. o& Medical Science", )onan,+

)oland. Author" Mlece# and Ga"ec#a are $ith %ept. o& -hemi"tr!, )onan *ni(. o&

i&e Science", )onan,+ )oland. Author iediel"#i i" $ith acult! o& -hemi"tr!, Adam

Mic#ie$ic *ni(. in )onan,+ )onan,+ )oland. Author Si$ul"#i i" $ith %ept. o&

eetable -rop", )onan *ni(. o& i&e Science", )onan,+ )oland. %irect in3uirie" to

author R!m"#i 4'mail r!m"#ipiotrump.edu.pl.

C()*+ 'nstitute of &ood echnolo-istsRdoi$ *).****/*01)2345*.*3(*(&urther reproduction without permission is prohi#ited

ate si$ni'cant medical costs (0mes and 8a*imoto +!!+). There&fore, the need to develop successful methods of prevention is anur$ent necessity. Se and Cu de'ciencies usually occur in re$ionswhere their content in the soil is etremely low (9e and an$ "--6;ayman +!!-).

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G. lucidum enriched with trace elements . . .

C$&oodChemistry

;ecent studies have demonstrated that G. lucidumcan be suc&cessfully enriched with selenium (Se), but also that it may biotrans&form inor$anic Se salts throu$h their inte$ration into proteins andpolysaccharides (/iedziels*i and others +!"). This 'ndin$ is im&portant if one considers that the biolo$ical role of Se is mainlymediated by its or$anic form, particularly selenoproteins. 1or e&ample, Se is *nown to be a reducin$ cofactor for some antio&idantenzymes and as a catalyst for the synthesis of active thy&roid

hormone (Schombur$ and 4ohrleD +!!#). of wheat bran, +> of corn Iour, and "> of

CaSHand moistened to J!> of water content usin$ distilled wa&ter and then sterilized at "+" KC for " h. The followin$ salts were

used in the eperiment: sodium selenite (/a+SeH ( to #>. Hnce thesubstrate was totally covered with the mycelium, it was trans&ferredto the cultivation chamber in which the temperature wasmaintained at + NC and relative humidity of air of #> to -!>.The cultivation was additionally irradiated with Iuorescent li$ht of

!! l intensity for "+ h a day. The $rowth facility was aerated insuch a way as to maintain CH+concentration below "!!! ppm. Theyield included whole fruitin$ bodies harvested successively as theymatured: after ! d (control), d (Se+Cu), # d (Se+Zn), or - d(Se+Cu+Zn).

Rea-ents0ll rea$ents, phosphoric acid, sodium hydroide, disodium hy&

drophosphate, and potassium dihydrophosphate (for phosphatebuffer preparation), were of analytical $rade (erc*, arm&stadt,9ermany). 8ater was puri'ed with a illi&O 0dvanta$e 0"!8aterFuri'cation System (erc* illipore, armstadt, 9er&many).Compressed ar$on $as of /&.! purity (--.--->) was obtained

from Ainde (Foznan,P Foland). 1or Cu, Zn, and Se spec&trometricdeterminations commercial standards (erc*) were ap&plied. Thestandard stoc* solutions were stored in $lass bottles at KC indar*ness. Aow concentration standards obtained by dilu&tion of thestoc* solutions were prepared daily. Falladium solution wasprepared from commercial palladium (as nitrate) chemicalmodi'ers (erc*).

Mushroom sample collection and preparationushrooms were collected when their biomass no lon$er

showed si$ns of further increase. The fruitin$ bodies were thenwei$hed, dried usin$ an electric drier SA8 ST (Fol&M*o,

P K

8odzisQaw Slas*i,R Foland) at ! + C for # h, wei$hed a$ainto determine the dry wei$ht, and then $round in a Cuttin$ ?ollill +!! (;etsch 9mbE, Eaan, 9ermany) for " min.

The powdered samples were sieved throu$h a !.!+ mm sieve,and a ".!!! !.!!" $ sample was etracted by " mol%A phos&

phoric acid in an ultrasonic bath at an ambient temperature for! min. Samples were then passed throu$h 'lter paper (washedwith +!! mA water and +! mA phosphate buffer). Sample pEwas adGusted to J.! to J. by the addition of "! mol%A ofsodium hydroide solution and 'nally the samples were dilutedto +! mA with phosphate buffer.

'nstruments1or Cu and Zn determination Iame, atomic absorption spec&

trometry (100S) Spectr00 ++! 1S (2arian, 0ustralia) was ap&plied with stoichiometric Iame acetylene (+.! A%min) and air(". A%min). Eollow cathode lamps (2arian, 0ustralia) wereused with the followin$ parameters for Cu: wavelen$th +.#nm, slit !., lamp current "! m0, and for Zn: wavelen$th +".-nm, slit ".!, lamp current m0, both with bac*$roundcorrection with a deuterium lamp. Calibration was provided forwater&based stan&dard solution without matri matchin$ usin$commercial standards (erc*). The coef'cients of variation

(r+) for calibration curves eceeded !.--. The determination

limits were !." m$%*$ with an uncertainty of about .!>(measured as ;S) for both determined elements.

1or Se determination, electrothermal atomic absorption spec&trometry (MT00S) Spectr00 +#!Z (0$ilent Technolo$ies, ul&$rave, 2ictoria, 0ustralia) with Zeeman bac*$round correction

C144 7ournal of &ood Science 6ol. 4*, Nr. 3,()*+

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Table 1Content (mg/kg dry weight) of particular Se forms in G. lucidumgrowing on substrates with Se(I)/Se(I)/Cu/!n addition"

Se(I) Se(I)

#lements addition (m$) Se Se9Cu Se9!n Se9Cu9!n Se Se9Cu Se9!n Se9Cu9!nb

!."ab

!.+.#a

".ab

!. !."a

!.! !.+a

!." !.+a

!.! !.+a

!.!control !.+a !.ab ab ".=b a a a a!." "+.Ja +. #.=b ".# #.+bc +.= +.+c !.= !."a !.! !."a !.! !.+a !." !."a !.!!.+ ++.a ".J "".#b +.! -.Jb +. .-b ".) !.+a !." !.a !.+ !.a !.+ !.+b !."

!. ".#a ".+-.-

=.! -.-

+. +.

".) +.-

!.= +.#

". ".=

!. !.=

!.+bc ab c

".,.Ja .a .Ja !.= !.b !."

!.J "-.Ja !.= -.ab . "+.ab .+ +.=b !. b !.

!. ab !.

"." a

!., ab

!.# +.! .= "J. . ".= +.= . .+ !.+ !." !. !.+Se

inorgSe

org

#lements addition (m$) Se Se Cu Se Cu !n Se Se Cu Se !n Se Cu !n

!. b !.! !.# ab9

Sea9!n9

ab 9 a ".! #.-a9

".- a9

9a 9control a ab !. .! ". ".-b !. #.#a a J.Ja !. =.-a !.+ab!." "+.=a +. #.-b ".# #.bc +.# +.c !.= ".=a +.= -.+a !.= -.a ".+ "".a .+!.+ ++.,a ".= "+.+b +.+ "!.+b +. ."b ".) "J.-a ".! "+.-a ".+ "+."a +.# "."a +.=

!. ).Ja !. "+.=

#. "".J

+.+ ."

".J "=.+

.= ".

".# "J. +. "".c

+."." ".!b ab c

".J a "=.a +!.Jab !.-

!.J +.a

"J.#ab .- ".-ab +. ."b +.-a +.

+!.-bc !.J

+J.!b +." #.Jc

!.# +.) .# . ".# +.J .# .+ .# . ".J +. ",.! +."#lements Se total Cu !naddition (m$)

Se Se9

Cu Se9

!n Se9

Cu9

!n Se9

Cu Se9 9

Se9

!n Se9

Cu9

!nCu !na -.= a +. -.J a ".+ -.# a a a a acontrol -."a ".! !.J "=.a . "."a ".# .#a ".! .+a ".ab ab b

!." +=.)a +. "#."b +. "=.#b .- ".-b ).- +.Ja .+ ++.=a J.J +#."a . +-."a ".-!.+ -.,a +.= +."b +.+ ++.b . "=.+b .= .=a . J.!a .! .Ja .# ".a ".!. )#."a .! +#.!b =.= +#.!b ." ".Jc .! +.-a .+ +=.a ""." J.!a . =.a "+.

!.J ,!."a +. ".b .= J.b +.# "".#c +., +=.+a +.= +J.=a ",.+ ".#a . -.=a ".!.# J#.+ .J =.= .! !.# .- "-.# ".# +-.! .+ ". "+.- ." .- ,+., "!.-

ean values (n=) standard deviations6 identical superscripts denote no si$ni'cant ().

The uncertainty of results was mainly produced by the samplepreparation step and was $enerally similar for 100S and MT00S.The traceability of both analytical procedures was controlled bycerti'ed reference material analysis (CS&&",

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C$&oodChemistry

traceability, owin$ to the lac* of any certi'ed reference mate&rials for determinin$ inor$anic Se species, the recovery of eachselenium species was determined by usin$ the standard&addition method. 0 recovery of -J> to "!> of each specieswas considered as satisfactory.

The concentrations of the or$anic Se fraction were calculatedas the difference between total Se concentration determined us&in$ MT00S and concentration of inor$anic seleniumcompounds determined usin$ EFACUE9U00S.

Statistical analysis and calculationsThe results were analyzed usin$ ST0T of the control level ofor$anic Se in the Se model, +> in the Se +Cu model, -> inthe Se+Zn model, and "-!> in the Se+Cu+Zn model.

iscussionThere is a $rowin$ interest in investi$atin$ the bioforti'cation of

cultivated mushrooms with trace elements. 9enerally, the substrateused for cultivation is only supplemented with one element at a sametime. 3nder such conditions, various mushroom species, includin$)leurotu" er!nii,)leurotu" o"treatu", and)holiota name#o(/iedziels*i and others +!"), have been shown to si$ni'cantlyta*e up and accumulate Se in their edible parts. oreover, our pilotstudy has shown that G. lucidummay ta*e up decidedly $reater Seconcentrations than other medicinal mushroom species

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C1:) 7ournal of &ood Science 6ol. 4*, Nr. 3,()*+

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such as Aroc!be aeerita, and 9ericium erinaceu"(/iedziels*i and others +!").

The co&occurrence of e7ual levels of Se, Zn, and Cu may poten&tially induce various interactions between these elements and altertheir upta*e by cultivated mushrooms. 0lthou$h, in this study, thesimultaneous presence of Cu and Zn decreased the accumulation ofSe in the fruitin$ bodies, its content in every studied model wasstill hi$h enou$h to represent a si$ni'cant source of this element

for human nutrition.

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6ol. 4*, Nr. 3, ()*+ 7ournal of &ood ScienceC1:*

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C$&oodChemistry

washin$ or coo*in$ (4alac and Svoboda +!!!), the G. lucidum$rown on substrate supplemented with !. m of each elementrepresents a hi$hly nutritional source of Se, Cu, and Zn.

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C1:( 7ournal of &ood Science 6ol. 4*, Nr. 3,()*+

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