metal accumulation by fungi

7/30/2019 Metal Accumulation by Fungi

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Journal of Industrial Microbiology, 13 (1994) 126-1309 1994 Society for Industrial Microbiology 0169-4146/94/$09.00Published by The Macmillan Press Ltd

Meta l accumulat ion by fung i : appl ica t ions in env ironmenta lb io t ech n o lo g y

J . M . T o b i n 1, C . W h i t e 2 a n d G . M . G a d d 21School of Biology, Dublin City U niversity , Dublin 9 , Ireland and 2D epartrnent of Biological Sciences, Un iversity of Dundee,Dundee DD1 4HN, Sco t land , UK

(Received 4 October 1993; accepted 4 Jan 1994)Key words : Fungi; Toxic metals; Biosorption; Pollution treatment; Immobilized biosorbent

SUMMARYFungi can accumulate metal and radionuclidespecies by physico-chemicaland biological mechanisms ncludingextracellular bindingby metabolites and

biopolymers,binding o specificpolypeptidesand metabolism-dependent ccumulation.Biosorptiveprocesses appear to have the most potential or environmentalbiotechnology. 'Biosorption'consists of accumulationby predominantlymetabolism-independent nteractions, such as adsorptive or ion-exchangeprocesses:the biosorptivecapacity of the biomasscan be manipulatedby a range of physical and chemical reatments. Immobilizedbiomassretains biosorptivepropertiesand possesses a numberof advantages for process applications. Native or immobilizedbiomass can be used in fixed-bed, air-lift or fiuidized bed bioreactors;biosorbed metal/radionuclide pecies can be removed for reclamationand the biomass regenerated by simple chemical reatments.

A number of processes may contribute to the uptake ofmetals by fungi and yeasts. Extracellular products mayremove metals from solution. These products include metab-olites such as sulfide or oxalic acid and a variety ofextracellular materials such as polysaccharides and extracellu-lar melanins. Fungi and yeasts can also produce a numberof proteins and polypeptides such as metallothioneins and7-glutamyl peptides in response to the presence of toxiclevels of certain metals in their e nvironme nt; some of theseare metal-specific and may b ind a substantial proportion ofthe intrace llular cont ent of metals such as Cu or Cd, therebyconferring resistance to the metals. Fungi and yeasts mayalso mediate metal removal from aqueous systems bychemical transf ormati ons such as redox changes or alkylationwhich can respectively precipitate or volatilize the metals[5]. In addition to these processes, fungal biomass may takeup metals by bi oaccumulation and biosorption. Bioaccumul-ation is the uptake of metal species by means of metabolism-dependent processes which may involve both transport intothe cell and partitioning into intracellular components; thishas been discussed elsewhere [2].B i o s o r p t i o n

To date, the most promising approach to metal removalby fungi is biosorption. Biosorption comprises binding ofmetals (or other solutes, colloids or suspensions) to thebiomass by processes which do not involve metabolicenergy or transport, although such processes may occur

Correspondence to: Dr G.M. Gadd, Department of BiologicalSciences, University of Dundee, Dundee DD1 4HN, Scotland, UK.

simultan eously where live biomass is used. It can the reforeoccur in either living or dead biomass. Several chemicalprocesses may be involved in biosorption, including adsorp-tion, ion exchange, co-ordination and covalent bonding.More than one process may contribute to uptake in any onesystem. The main chemical groups in biomass which areable to partake in biosorption are electronegative groupssuch as hydroxyl or sulfhydryl groups, anionic groups suchas carboxyl or phosphate groups and nitrogen-containinggroups such as amino groups. Carboxyl and phosphategroups are considered to be important binding sites formany toxic metals [18] while the a mino groups of chitinwere found to be a major site of thorium uptake in R h i z o p u sa r r h i z u s . The initial thorium uptake comprised a rapidadsorption/ion exchange component which was followed bya slow covalent component [22]. The three-dimensionalstructure of binding sites also appears to be significant asthe ionic radius affected the biosorption of ions by R.a r r h i z u s [15]. The cell walls of fil amentous fungi and yeastsappear to have the major role in biosorption due topossession of numerous upta ke sites of the types me ntione dabove. Nonetheless, the interior of the cell also containsmany components which bind metals so that treatmentswhich permeabiliz e the cell, such as grinding [15], det ergents[3] or HC HO and HgC12 [14], incr ease the uptak e of anumber of metals and radionuclides. These methods mayalso expose active sites in the cell wall which could contribu teto increased uptake. Unlike many of the other processes formetal removal using microbes, fungal biosorption can removesuspended solids as well as solutes. A s p e r g i l l u s n i g e r biomasstook up copper, lead and zinc sulfides onto mycelial surfacesand several fungi could adsorb solid metal compounds fromacid mine waters [27].


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127Upt ake of metals from solut ion by fungi is subject to

interference from a num ber of subs tances and chemicalcondit ions . Bioaccumula t ion and biosorpt ion o f metals canbe inhibi ted by the presence of anions such as phosphateswhich complex or precipi ta te them and render them unavai l-able to the cellular binding sites for metals [16]. Cations,including H +, can a lso interfere by blocking potent ia l bindings i tes . Both bioaccumulat ion and biosorpt ion of cat ions suchas Cu 2+, Cd 2+, Zn 2+, M n 2+ and Co z+ are decreased by alow pH [2]. The presence of other cat ions may also exert as imilar effect through competi t ion for binding s i tes [17].However , the pH e f fec t i s dependen t on the chem is t ry o fthe metal species and binding s i tes . For example , thoriumbiosorp t ion by R. arrhizus biomass was higher a t pH 4 than2, apparent ly due to the shif t of prevalent ion to hydrolyzedspecies from fr ee Th 4+, and the distribu tion in the cell-wallwas also altered [22],

The chemical composi t ion of the fungal wall is s t rongly

dependent on the cul ture condit ions and this may inturn affect biosorpt ive propert ies . For example , thoriumbiosorpt ion by inact ive R. arrhizus biomass was greaterwhen cel ls were grown on s imple than on complex medium[3]. The cul ture phase a t harves t may exert s imilar effects ,with uptake by biosorpt ion and bioaccumulat ion beinggeneral ly less a t la ter growth phases as a resul t of chemicalchanges in the mycel ium. The presence of toxic metals inthe growth medium can a lso a l ter the cel l wal l composi t ion,sometimes resul t ing in product ion of melanins and increasedmetal-binding capaci ty [2] .Biomass immobi l iza t ion

A num ber o f inves t igat ions of fungal biosorpt ion havefocussed on biomass in i ts nat ive s ta te and numerous s tudieshave reported the metal uptake characteris t ics of a varie ty offreely suspended organisms under varying solution condit ions[1,3,6,14,15]. However, immobil ized or pel le ted biomass

Fig. 1. Scanning electron micrographs of (A) Cladosporium cladosporoides mycelial pellet (bar = 1000 p,m); (B) Aspergillus nidulansmycelial pellet (bar = 1000/zm); (C) m ycelial network o f A. nidulans pellet (bar = 10 tzm); (D) immobilized Rhizopus arrhizus in polyvinylformate (biomass loading 50%) (bar = 100/zm). Fig. I(D) courtesy of Dr J.C. Roux, CE REM -DE M-S ECM Lab., Centre d'Etu des

Nucleaires, Grenoble, France,


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12 8o f f e rs c o n s i d e r a b l e a d v a n t a g e s i n t e r m s o f h a n d l i n g ,s o l i d - l i q u i d s e p a r a t i o n a n d e a s e o f s c a l e - u p . S e v e r a l s t u d i e sh a v e d e s c r i b e d t h e p r o d u c t i o n o f b i o m a s s p e l l e t s ( F i g . 1( A - C ) ) d u r i n g g r o w t h o f s e v e r a l f i l a m e n t o u s f u n g a l c u lt u r e s[ 1 2, 1 3, 1 9] a n d t h e u s e o f i m m o b i l i z i n g s u p p o r t m a t r i c e sr a n g i n g f r o m n a t u r a l p o l y s a c c h a r i d e g e ls t o c o a l , s a n d , f o a ma n d a r a n g e o f s y n t h e t i c p o l y m e r s [ 7 - 9 , 2 3 ,3 0 ] . A l o n g w i t hm e c h a n i c a l s t r e n g t h a n d d u r a b i l i t y , k e y c o n s i d e r a t i o n s i nu s i n g i m m o b i l i z in g m a t r i c e s a r e t h e b i o m a s s l o a d i n g a t t a i n -a b l e a n d t h e d e g r e e o f b l o c k i n g o f th e b i n d i n g s i te s b y th ei m m o b i l i z i n g m a t e r i a l .

F o r R. a r r h i z u s i m m o b i l i z e d i n p o l y v i n y l f o r m a t e ( F i g .I ( D ) ) , b i o m a s s l o a d i n g s o f u p t o 8 8 % w e r e r e p o r t e d b u tw i t h a c o n c o m i t a n t r e d u c t i o n i n o v e r a l l m e t a l - b i n d i n gc a p a c i t y o f 3 0 % , b o t h c a l c u l a t e d o n a d r y w e i g h t b a s i s [ 23 ].A l g i n a t e e n t r a p m e n t t e c h n i q u e s a r e s i m p l e , n o n - to x i c , a n da r e w i d e l y u s e d f o r c e l l i m m o b i l i z a t i o n . C e l l l o a d i n g s o f u pt o 7 0 % o f th e d r y w e i g h t h a v e b e e n a c h i e v e d w i t h o u tr e p o r t e d l o s s i n m e t a l b i n d i n g d u e t o t h e i n h e r e n t p o r o s i t yo f th e g e l b e a d s [1 3] . U n d e r c e r t a i n c o n d i t i o n s t h e a l g i n a t em a t r i x i t s e l f m a y c o n t r i b u t e s i g n i fi c a n t ly t o m e t a l b i n d i n g .C a d m i u m r e m o v a l e f f ic i e n c ie s i n e x c e s s o f 7 0 % h a v e b e e no b s e r v e d d u e t o a l g i n a te a l o n e [ 8 ], a l t h o u g h u r a n i u m b i n d i n gu n d e r s i m i l a r ' c o n d i t i o n s w a s r e p o r t e d t o b e n e g l i g i b l e [1 3] .I n g e n e r a l , h o w e v e r , t h e l o w m e c h a n i c a l s t re n g t h o f a l g i n a t eg e l s t o g e t h e r w i t h t h e r e v e r s i b i l i t y o f t h e c r o s s l i n k i n g [8 ]m a y l i m i t t h e i r r a n g e o f a p p l i c a t i o n . P o l y a c r y l a m i d e t y p eg e ls h a v e b e e n w i d e l y u s e d i n l a b o r a t o r y - s c a l e b i o s o r p t i o ns t u d i e s w i t h v a r y i n g c e l l l o a d i n g s a n d m i n i m a l r e p o r t e dl o s se s o f b i n d i n g c a p a c i t i e s b u t t h e y a r e u n s u i t a b l e f o r l a r g es c a l e p r o c e s s e s b e c a u s e o f t h e t o x i c i t y a n d c o s t o f t h em a t e r i a l s a n d t h e l i m i t e d m e c h a n i c a l s t r e n g t h o f t h e r e s u l t in gb i o s o r b e n t [ 9 - 11 ] .

U n d e r s u i t a b l e g r o w t h c o n d i t i o n s c e r t a i n f u n g i , i n c l u d i n gAs pe r g i l l u s , Rh i z opus , a n d Pe n i c i l l i um s p e c i e s , p r o d u c es p h e r i c a l m y c e l i a l p e l l e t s w h i c h h a v e b e e n u s e d i n b i o s o r p t i o ns t u d i e s ( F i g . 1 ( A - C ) ) [ 1 3 , 1 9 ] . H i g h m e t a l u p t a k e l e v e l s( e x c e e d i n g th o s e o f i o n e x c h a n g e r e s i n s u n d e r c e r t a i nc o n d i t i o n s ) a n d g o o d d e s o r p t i o n c h a r a c t e r i st i c s h a v e b e e nr e p o r t e d a l t h o u g h t h e p o t e n t i a l f o r u s e i n m u l t i p l e u p t a k e /d e s o r p t i o n c y c l e s h a s y e t t o b e d e m o n s t r a t e d [ 1 3, 2 9] .Bi os or p t i on r e ac to r c on f i gur a t ions

I m m o b i l i z e d b i o s o r b e n t s a r e a n a l o g o u s t o i o n e x c h a n g er e s in s o r c a r b o n a d s o r b e n t s a n d t h e r e m o v a l o f m e t a l i o n sf r o m s o l u t i o n b y b i o s o r p t i o n i s e s s e n t i a l l y a c o n v e n t i o n a ls o l i d - l i q u i d c o n t a c t i n g a n d s e p a r a t i o n p r o c e s s . C o n v e n t i o n a ls o l i d - l i q u i d p r o c e s s i n g e q u i p m e n t f a l ls i n to t h e t w o c a t e g o r i e so f s t i r r e d a n d p a c k e d b e d r e a c t o r s a n d b o t h h a v e b e e n a p p l i e di n l a b o r a t o r y a n d l a r g e r - s c a l e b i o s o r p t i o n i n v e s t i g a t i o n s[9 ,15 ,25 ,28] .

S t i r r e d t a n k r e a c t o r s m a y b e o p e r a t e d i n b a t c h o rc o n t i n u o u s m o d e a n d a p p l i c a t i o n s t o b i o t e c h n o l o g y r a n g ef r o m c l a s s i c al a c t i v a t e d s l u d g e s y s t e m s t o l a b o r a t o r y s c a l eb a t c h i n v e s t i g a t i o n s . T o d a t e , a l l f u n g a l s y s t e m s r e p o r t e da r e o f s m a l l s c a l e a n d u s e s u s p e n d e d o r i m m o b i l i z e d f u ng a lb i o m a s s , o r b i o f i lm s . M a n y s t u d i e s r e p o r t u p t a k e l e v e ls f o rd i f f e r e n t m e t a l / b i o m a s s s y s te m s ( T a b l e 1 ) a n d a d s o r p t i o n

i s o t h e r m s a r e f r e q u e n t l y u s e d t o q u a n t i f y t h e e q u i l i b r i u mr e l a t i o n s h i p b e t w e e n t h e u p t a k e a n d s o l u t i o n c o n c e n t r a t i o n[ 3 ,1 5 , 23 ] . S o m e t y p i c a l is o t h e r m s e x h i b i t i n g s a t u r a t i o nb e h a v i o r a r e i l l u s t r a t e d in F i g . 2 . A l i m i t a t i o n o f s t i r r e dt a n k s y s t e m s is t h e n e e d f o r a s o l i d / l i q u i d s e p a r a t i o n s t a g ep r i o r t o s u b s e q u e n t r e g e n e r a t i o n / m e t a l r e c o v e r y o r d i s p o s a ls t a ge s . I n c o m m e r c i a l f u l l -s c a l e p r o c e s s e s , s e d i m e n t a t i o n i su s u a l l y t h e m e t h o d o f c ho i c e w h e r e a s i n s m a l l e r e x p e r i m e n t a lu n i ts m o r e e x p e n s i v e f i l t ra t i o n o r c e n t r i f u g a t i o n m e t h o d sa r e m o r e c o m m o n .

P a c k e d b e d s y s t e m s o b v i a t e t h e n e e d f o r a d d i t i o n a l so l i d /l i q u i d s e p a r a t i o n s y s t e m s a n d a r e w e l l s u i t e d t o c o n t i n u o u sf l o w a d s o r p t i o n a n d r e g e n e r a t i o n c y c l e s . I n c r e a s i n g l y ,b i o s o r p t i o n r e s e a r c h i s f o c us s i n g o n c o n t i n u o u s s y s t em s f o ri n d u s t r i al a p p l i c a t io n s . A k e y d e s i g n f e a t u r e o f t h e s e s y s t e m si s t h e b i o r e a c t o r r e s i d e n c e t im e a n d r e c e n t r e p o r t s h a v eh i g h l i g h t e d t h e f a c t t h a t , a l t h o u g h b i o s o r p t i o n i s a r a p i dp r o c e s s , i n s uf f ic i e n t r e s i d e n c e t i m e s m a r k e d l y d e c r e a s e m e t a lr e m o v a l l e v e ls [ 9 ,3 0 ]. R e d u c e d u p t a k e e f f ic i e n c ie s r a n g i n gf r o m 3 0 7 0 % o f th e b a t c h s y st e m v a lu e s h a ve b e e n o b s e r v e df o r c o n t i n u o u s f l o w s y s t e m s u s i n g f u n g a l m y c e l i a l p e l l e t s

T A B L E 1Metal uptake capacit ies of selected fungiBiomass Meta l Uptake* pH range Refe rence

mmol g-~ %Saccharomyces Sr2+ 0.24 20.9 5.5 1cerevisiae Th 4+ 0.27 12.0 0-1.0 28

UO22+ 0.63 15.0 4.0 14Rhizopus C r3+ 0.59 30.7 3.5-4.0 15arrhizus L a3+ 0.35 4.9 3.5-4 .0 15

Cu 2+ 0.2 5 1.6 3.5-4.0 15A g2+ 0.5 5.4 4.0 2Cd z+ 0.27 3.0 3.5-4 .0 15H g2+ 0.2 9 5.8 4.0 2Pb 2+ 0.50 10.4 3.5-4.0 15UO22+ 0.82 19.5 3.5-4.0 15Th 4+ 0.79 18.5 4.0 22Th 4+ 0.50 11.6 0-1.0 3

Aspergillus Th 4+ 0 .2 8 13 .8 0 -1 .0 3niger UO2 2+ 0.9 21.4 5.8 29

Penicillium Th 4+ 0 .49 11 .4 0 -1 .0 3italicumPenicillium Th 4+ 0.84 19.5 0-1.0 3chrysogenumPenicillium C1 UO22 + 0 .71 17 .0 4 .0 2

*The maximum uptake given in the reference ci ted; molar andpercentage concentrat ions both relate to dry weight of biomass.Referral to original references is recommended for experimentaldetai ls relat ing to metal concentrat ions, contact t imes, and biomassdensity.


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129

250 B C2009_?

E 150"Eo = 1 o o -

50-E

F0 ,0 0.2 0.4 0.6 0.8 1.0

Metal concentration raM)Fig. 2. Biosorption equilibria for some metal cations by fungi andyeasts. The graph shows strontium biosorption by (A) freeze-driedR. a r rh i zu s biomass and (B) denatured S a c c h a ro m y c e s c e re v i s i a ebiomass [1], (C) copper biosorption by Mu c o r c i rc in e l l o id e s biomass(Gadd and de Rome, unpublished), (D) thoriumbiosorption by S.cerevis iae biomass [6], (E) strontium biosorption by live S. cerevis iae[1] and (F) copper biosorption by live S. cerevis iae at pH 2 (Whiteand Gadd, unpublished). Data were obtained with a biomassconcentration of 1.0 mg dry wt m1-1 and a contact time of 1 h in(C) and (F); other conditions are given in the original publications.Curves (A)-(C) and (E) were obtained at pH 5.5 and (D) at pH


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130u n s a t u r a t e d d e s o r b e n t [ 4] . A s t h e c a p a c i ty o f f u n g al b i o m a s sf o r m e t al s is st r o n g ly d e p e n d e n t o n t h e b i o m a s s c o n c e n t r a t i o nd u r i n g b i o s o r p t i o n , i n c r e a s i n g t h e b i o m a s s c o n c e n t r a t i o nm a y i n c r e a s e t h e t o t a l r e m o v a l a t th e c o s t o f r e d u c e d l o a d i n gp e r u n i t o f b io m a s s [2 ] a n d r e d u c e t h e c o n c e n t r a t i o n o f a ne l u t e d m e t a l p r o d u c t . T h i s e m p h a s i z e s a s i g n i f ic a n t p o i n tt h a t , in a n y p r a c ti c a l a p p l i ca t i o n , t h e d e v e l o p m e n t o f m e t a lb i o s o r p t i o n m u s t b e c o n s i d e r e d a s p a r t o f a n o v e r a l l m e t al -r e m o v a l o r m e t a l - r e c l a m a t i o n p r o c e s s .

A C K N O W L E D G E M E N T S

J . M . T . a n d G . M . G . g r a t e f u ll y a c k n o w l e d g e r e se a r c hs u p p o r t f o r c o l l a b o r a t i v e i n t e r c h a n g e f r o m t h e B r i t i s hC o u n c i l / E O L A S J o in t R e s ea r c h S c h e m e .

R E F E R E N C E S

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2 G a dd, G .M . 1993. In te ra c t ions of fungi w i th toxic m e ta l s . Ne wPhyto l . 124: 25-60 .

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8 Kuhn , S .P . a nd R .M . Pf is te r. 1989 . Adso rpt ion o f m ixe dm e ta l s a nd c a dm ium by c a lc ium -a lg ina te im m obi l i z e d Zoogloearamigera. Appl . Mic robio l . B io te c hnol . 31 : 613-618.

9 Ma c a skie , L .E . a nd A .C .R . De a n. 1989. Mic robia l m e ta bol i sm ,de solubi l i z a t ion , a nd de pos i t ion of he a vy m e ta l s : m e ta l up ta keby im m obi l i z e d c e l l s a nd a ppl ic a t ion to the t r e a tm e nt of l iqu idwa s te s. In : B io logic a l Wa s te Tre a tm e nt (Miz ra hi , A . , e d . ) , pp .159-201, Alan R. Liss , New York.

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