Indian Journal of Experimental Biology

Vol. 41, September 2003, pp. 967-971

\
~

Biorecovery of gold
Ronald Eisler*
U.S. Geological Survey , Patuxent Wildlife Research Center, Laurel, Maryland 207084019, USA

Recovery of ionic and metallic gold (Au) from a wide variety of solutions by selected species of bacteria, yeasts. fungi.
algae. and higher plants is documented. Gold accumulations were up to 7.0 g/kg dry weight (OW) in various species of
bacteria, 25.0 g/kg OW in freshwater algae, 84.0 g/kg OW in peat. and 100.0 g/kg OW in dried fungus mixed with kerati-
nOlls material. Mechanisms of accumulation include oxidation, dissolution, reduction. leaching, and sorption. Uptake
patterns are significantly modified by the physicochemical milieu. Crab exoskeletons accumulate up to 4.9 g Au/kg OW;
however, gold accumulations in various tissues of living teleosts, decapod crustaceans, and bivalve molluscs are negligible.

Keywords : Biorecovery of gold, Gold uptake

Extraction of gold from solutions is under active
investigation using a variety of physical, chemical,
and biological processes. Recovery of ionic gold from
dilute solutions usually involves either precipitation
by zinc dust, carbon adsorption, solvent extraction, or
ion exchange resins. All of these are of low selectivity
and comparatively expensive I.2. Chemical methods
for the recovery of gold from ores include cyanidation
and thiourea leaching, which present environmental
and health risks3.4. Biorecovery of dissolved gold
from solution presents fewer environmental risks than
chemical methods, and is documented for
. .
mIcroorganisms 25-20
' ,a Igae 1421 . , water lernsl' 22 , peat-?3 ,
4
alfalfa , seaweeds2. 12.18.24.25, fungi 2. 18.26.29, yeasts l4 , and
crab exoskeletons 3o . This account briefly reviews the
potential of living and dead plants and animals to
accumulate gold from solution, and some of the
processes involved - including biooxidation,
dissolution, bioreduction, bacterial leaching, and
biosorption.
Gold uptake by microorganisms, fungi, and higher
plants
Biomining processes are llsed successfully on a
commercial scale for the recovery of gold and other
metals, and are based on the activity of obligate
chemoautolithotropHic bacteria that use iron or sulfur
as their energy source and grow in highly acidic
media 13. Biooxidation of difficult to treat gold-bearing
arsenopyrite ores occurs in aerated, stirred tanks and
*For correspondence:
Email: ronald.cisler@usgs.gov
Fax : 301-497-5744
Phone : 301497-5724
rapidly-growing, arsenic-resistant bacterial strains of
Thiobacillus ferrooxidans (Beijerinck), LeptospiriLlium
ferrooxidans (Beijerinck), and Thiobacillus ferrooxidans
(Beijerinck). These bacterial species obtain their
energy through the oxidation of ferrous to ferric iron
(T. ferrooxidans, L. ferrooxidans) or through the
reduction of inorganic sulfur compounds to sulfate
(Thiobacillus spp.). Monetary costs of biooxidation
are reported to be about 50% lower than roasting or
pressure oxidation 13. Adding Thiobacillus
ferrooxidans into the thiourea leaching solution
produces a 20% increase in the extraction of gold.
The reaction describing gold dissolution in an acidic
solution of thiourea in the presence of ferric ion IS
described by Kai et a/.f:> as :
Au + Fe3+ + 2CS(NH 2h ~ Au[CS(NH 2hf+ + Fe2+
The use of bacteria in pretreatment processes to
degrade recalcitrant gold-bearing arsenopyrite ores
and concentrates is well established7 19. Recalcitrant
ores are those in which the gold is enclosed in a
matrix of pyrite and arsenopyrite, and cannot be
solubilized by direct cyanidation. Bacterial
decomposition of arsenopyrite assists in opening the
molecular mineral structure, permitting access of the
gold to cyanide. However, greater quantities of
cyanide are required to solubilize gold after bacterial
treatment when ores contain high quantities of gold. A
possible cause of this excessive cyanide is the
presence of the enzyme rhodanese, produced by
Thiobacillus caldus (Beijerinck), a common species
of bacterium encountered in biooxidation facilities l 9 .
Optimum microbiological leaching by Thiobacillus
spp. and Sulfolobus spp. of refractory sulfide ores for
968 INDI A N J EXP BIOL , SEPTEMB ER 2003
recovery of go ld in tanks is poss ible under controlled
conditions of pH, di ssolved oxygen, carbon di ox ide,
sul fur balance, redox potenti al, tox ic metal
concentrati ons, and rate of leachin g7.
Several species of Fe3+ -reducing bacteri a (Bacteria
spp., Archaea spp.) can precipitate go ld by reducing
Au' + to Au' with hydrogen as the electron donor"o.
Rate of bacteri al ox idati on by ThiobacilLus
fe rrooxidans and Leptosp irillium fe rrooxidans of
three South Afri can refractory go ld ores of varying
go ld-arsenopyrite co mposition was dependent mainl y
on crystal structure R These go ld ores were c1 ass ifi ed
as refractory due to th e presence of go ld inclusions in
arsenopyrite and pyrite, and submi croscopi c gold
ma inl y in arsenopyrite. Refractory go ld occ urs at sites
whi ch are preferenti all y leached by th e bacteri a. The
rate of go ld liberati on fro m sul fides is enhan ced
durin g th e earl y stages of bac teri al ox idati on. Defects
in crys tal structure influence the rate of bioox idati on
and is directl y related to th e crystal stru cture of th e
sulfid e mineral, the crystall og rapHi c ori entati on of th e
exposed surfaces, and diffe rences In chemi cal
composIti on and mechani ca l dev iat ions in the
crys tals x. Pretreatment of refractory go ld concentrates
with the bacterium Thiobacilllls fe rrooxidans
ul timately results in sulpHur and sulpHide ox idati on
by fe rri c ion s from bacteri al ox idati on of ferrou s ions.
The max imum co ncentrati on of attac hed Thiobacillus
increases with increasing co nce ntrati on of Fe 2+ and
decreases with increasing size of the refrac tory go ld
concentrate particles '6 . In Chile, whi ch produced
30,000 kg of go ld in 1990, Thiobacillus ferrooxidans
was used to recover go ld from a co mple x ore under
laboratory conditi ons9 . The ore contained 8.2% Fe,
0.78% Cu, 0.88 % As, and 3. 5 g Au/ton, with pyrite,
hematite, arsenopyrite, and chalcopyrite as the mai n
metal- bearin g minerals. Initi al go ld recovery by
co nve nti onal cya nid ati on on a cru shed ore sampl e was
54%; co ncentrati on by fl otati on improved reco very to
56%. Conce ntrated sampl es (17 .0 g Au/ton) were
leached in reactors at p H 1.8. In th e presence of
bacteri a, all di ssolved iron was present as ferri c ion;
gold recovery by cyanidati on increased fro m 13% fo r
th e initi al concentrate to 97 % after 10 days of
bacteri al leachin g. To furth er increase go ld recovery,
fl otati on tailings were submitted to cyanid ati on9 .
Some mi croorga nisms isolated from go ld-bea rin g
depos its are capabl,e of di ssolving go ld ; di ssolution
was aided by the prese nce of asparti c acid, histidin e,
serine, alanine, glyc ine, and metal ox idants5 . Bacleri f-
a nn go ld is well know n, with uptake of Au3+ from
chl oride soluti ons doc umented fo r at least seven
genera of fres hwater cyanobacteria3 1. So me
bacteriform go ld is bi ogeni c - the res ult of
precIpitati on by bac teri a - and may be usefu l
indicators of gold deposits and of processes of go ld
acc umul ati on. PLectonema terebrans Born et, a spec ies
of fil amentous marine cyanobacteria, accumul ates
go ld in its sheath fro m an aqu eo us solu tion of AuCl 3 .
Sheaths are among th e few stru ctures likely to be
preserv ed in so me form in mi crofossi ls of ancient
bacteri a. In marine medi a, it is ex pec ted th at AuCI3
(2.0 g Au/l ) will fo rm AuCI ~ , Au' ; , and AuCi ;31.
Biosorption of Au3+, as AuCi ~ , by dri ed Pseudomonas
strains of bac teri a was inhibited by palladium, as Pd 2+,
and possibl y other metal ions 10 .
Go ld adsorpti on fro m cyanide solutions by dead
bi omass of bacteri a (Bacillus subtilis), fun gus
(Penicillium chrysogenum Thom), or seaweed
(Sa rgassum flu itans Linnae us) at p H 2.0 were 1.8 g
Au/kg OW fo r bacteri a, 1.4 g/kg OW for fun gus, and
0.6 g Au/kg OW fo r seaweed. Ani oni c AuC ;
adso rpti on was th e major mechani sm in go ld bioso r-
ption fro m cya nide so luti ons, being mos t efficient at
lower p H va lues 2 . L-cysteine increased go ld-cya nide
bi oso rpti on of Bacillus, PenicilliulIl, and Sa rgassum l R
At pH 2, the max imum go ld uptakes were 4.0 g Au/kg
OW fo r bac teri a, 2.8 g/kg fo r fungus, and 0.9 g/kg fo r
seaweed, or 150-250% greater than in the absence of
cysteine. The ani on ic gold cya nide species were
adsorbed by ioni zable fun cti onal groups on cys teine-
loaded biomass; depos ited gold coul d be eluted fro m
go ld-loaded biomass at p H 5.0 18
Go ld-resistant strains of bac teri a th at also
acc umul ate go ld are doc umented, although the
fundamenta l mechani sm of resistance to go ld in
mi croorgani sms is not known or und erstood 15. One
strain of Burkholde ria (Pseudomonas) cepacia
Burkholder co ntained millimolar concentrati ons of
Au+ thi olates. Burkholde ria cells were large,
accumul ated polyhyroxybutyrate and gold, and
excreted thi orin , a low molec ul ar weight protein into
the cultu re medium . Thi s effect was not observed with
th e Au3+ co mpl exes tes ted, whi ch were reduced to
metalli c go ld in the medium. Gold-res istant strains of
fun gi and heterotrophic bacteri a are also kn ow n ' 5 .
Rapid recovery of go ld from go ld-thi ourea
solutions was doc umented fo r waste biomass of yeasts
(Saccha romyces cerevisiae), cyanobacteri a (Sp iruLina
platensis [Nordst]), and bac teri a (Streptomyces
erythralus [Waks manl)' 4 The process is p H-
 EISLER : BIORECOVERY OF GOLD
dependent for yeast and bacteri a, and pH-indepe nde nt
fo r Spirulina. O f all stra in s of mi croo rgani sms
examin ed, Spirulina platensis has the hi ghest affinit y
and capac ity for gold , eve n at lo w pH values. G o ld
uptake by Spirulina was 7 .0 g Au/kg bi o mass OW in
1-2 hr at p H 2. 0, and abo ut 3.0 g A u/~ g OW in 15 min
14
atpH 2 throu gh 7 .
Metabolicall y acti ve fun gal cell s of Aspergillus
f umigatus Fresen and A. niger Ti egh re mo ved gold
from cyanide leach liquor of a Brazili an gold extracti on
pl ant more effi cientl y than did dri ed fun gal bio mass or
other species of Aspergillus tested . These two species
of fung i removed 35 to 37% of go ld from so lutio ns
containing 2.8 mg A u/I in 84 hr26. Gold re moval fro m
cyanide-containing solutio ns is documented for a strain
of Aspergillus niger, a fun g us iso lated from the gold
26 28
extracti on pl ant at Nova Linda, BraziI - . The leach
liquor contained, in mg/I , 18 1.0 cyanide, 1.3 go ld , 0 .4
sil ver, 7. 1 copper, 5.2 iron, and 4 .5 zinc. After 60-72 hr
of incubati o n, A. niger removed from so luti o n,
probabl y by adsorpti o n, 64% o f the go ld, I 00% of the
si lver, 59% of the copper, 80% of the iron, and 74% of
the zinc; all gold was re moved after 120 hr. Use of thi s
fungus to develo p a bi oprocess to reduce metal and
cyanide levels as well as recovery of va lu abl e metals
shows promj se 26-28. Uptake pattern s of gold from Au +
3
soluti ons by dead fungal bi o mass fo llowed
mathemati cal uptake mode ls of Lang muir and Freu-
ndlich; bi o mass was prepared from the fruiting body of
a mu shroo m co ll ected fro m the forests of Kerala,
29
Indi a . Dri ed fungus, Cladosporium cladosporoides
Fresen, mi xed w ith keratino us materi a l of natural
origin to form a bead, proved effecti ve in absorbing
l2
gold fro m so lutio n . The bi osorpent beads adsorbed
100.0 g Au/kg beads fro m a soluti o n containing 100 .0
mg Au/ I. Max imum bi osorpti o n of 80% occ urred at
acid pH ( 1-5) in less than 20 min . The bi osorpe nt beads
degraded in so il in about 140 days . The beads also
removed 55 % of the go ld from e lectropl ating so luti o ns
containing 46.0 mg Au/I , w ith observed go ld loading
capacity of 36.0 g/kg beads 12. Dri ed bi osorpents
encapsul ated in po lysul fo ne were prepared fro m
microorgani sms iso lated fro m pri stine o r ac id mine
drainage enviro nme nts " . Biosorpent materi a l ri ch in
exopolysaccharides fro m the ac id mine drainage site
bo und Au 3+ three times mo re e ffec ti vely th an did other
materi als, and removed 100% of the A u3 + from
soluti ons containing 1.0 mg Au/ I within 16 hr at 23C
andpH 3.0.
Algal ce ll s, ali ve o r dead , rapidl y accumul ate A u3+
and begin to reduce it to A u and A u+ w ithin 2 d ays 33 .
969
Uptake of Au 3+ by Chlorella vulga ris Be ij erinc k, a
uni cellul ar green alga, from soluti o ns conta ining 10.0
21
o r 20.0 mg A u 3+/l is documented . Chlo rella
accumul ated up to 16.5 g Au/kg OW . In acti vating the
a lgal cell s by variou s treatments resulted in so me
enh ancement in uptake capac ity o ver the pri stin e
cell s. In acti vati o n by heat treatment yie lded up to 18.8
g/kg DW ; fo r alk ali treatment, thi s was 20. 2 g/kg
OW ; fo r form aldehyde treatment, 25.5 g/k g OW ; and
fo r acid treatment, 25 .4 g/kg OW . E le me nta l go ld
(A u") was measured by X-ray pho toe lectro n
spectroscopy o n the cell s urface, indi catin g th at a
21
reducti o n had occurred . Studies with li vin g Chlor-
ella vulga ris suggest th at accumul ated Au 3+ is rap id ly
15
reduced to A u+, fo ll o wed by a slo w reducti o n to A U .
With dead a lgae, A u ini tiates a seedin g process whic h
res ults in the formati o n of e leme ntal gold .
Sequeste rin g meta l io ns usin g li ving o r dead pl ants
is a pro posed eco no mi cal means o f re mov ing go ld
and oth er meta ls via intracellul ar acc umul ati o n o r
s urface adsorpti o n. H owever, in the case of li ve
pl ants, thi s is freq ue ntl y a re lati vely slow and time-
consumin g process. No nli vin g pl ant materi a l fo r
s urface adsorpti o n offers several ad va ntages over live
pla nts, in cl udin g redu ced cost, greate r avail abil ity ,
eas ie r regenerati o n, and hi g he r me ta l spec ific ity4. In
South Afri can minin g e fflu e nts, go ld us uall y ranges
betwee n I and 10 mg/I. In studi es of 180-m in
durati o n, dri ed red water fe rn s, Azalla .filiculoides
La marc k, re moved 86 to 100% of A u 3+ fro m ini tial
3
so luti o n of 2 to 10 mg Au +/l , in creas ing with
increased initi a l concentrati o n o f A u 3+ (ref. 22). The
bio mass gave >95 % re moval e ffic iency at all bi o mass
concentrati o ns measured . Optimum (99.9 %) removal
of gold occUlTed within 20 min at pH 2, 42% remova l
at pH 3 and 4, 63 % at p H 5, and 73% re moval at p H
6; remova l effic iency see med indepe ndent of
te mpe rature 22 . Simil ar res ults were o bserved w ith fo ur
spec ies of gro und dri ed seaweeds (Sargassum sp.,
Gracila ria sp ., Eisenia sp ., and Ulva Sp. )25 Treated
seawecds re moved 75-90% of the go ld within 60 min
3
at pH 2 fro m so luti o ns co ntaining 5.0 mg A u +/l . Go ld
3
(A u +) ca n be sequestered f ro m ac id so luti o ns by dead
bi o mass of a brown alga, Sargassum na(ans
(Linn aeus), and depos ited in its e leme ntal fo rm , A U 24 .
The ce ll wa ll of Sa rgassum was the maj o r loca le fo r
go ld depos iti o n, w ith carbo ny l g ro ups (C = 0 ) pl ay ing
a maj o r ro le in bindin g, and N-conta ining groups a
lesser ro le. Lik e activ ated carbo n, th e biomass of
Sa rgassum natans is ex tre me ly po rou s, reportedl y
more tha n most bi o materi als, and acco unts, in part ,
970 INDIAN J EXP BIOL, SEPTEMBER 2003
fo r its ab ility to accumulate go ld 24 . Dried ground
shoots of alfalfa, M edicag o sa/i va Linnaeus, were
effective in removing go ld from solution 4 .The
acc umulation process in vo lved th e reduction of Au 3+
to colloidal Au', and was most effici ent at elevated
temperatures and ac id pH. In so lutions containing
60 mg Au )' /I, abou t 90% of the Au 3+ was bound to
dri ed alfalfa shoots in abo ut 2 hI' at pH 2 and 55C.
The mechanism to acco unt for thi s phenomenon is
unknown , but may in vo lve red ucti on of Au 3+ to Au +,
the latter being un stabl e in water to form Au' and
Au 3+ (ref. 4). Dri ed peat from a Brazilian bog
acc umulated up to 84.0 g Au/kg OW within 60 min
from so luti ons conta ining 30.0 mg Au3+/1 (ref. 23).
Gold uptake by aquatic macrofauna
Except for crab exoskeleton s, go ld recovery from
the medium by various species of li ving molluscs,
cru staceans, and fi shes is neg li gible.
Cert ain chitinous materials, such as exos keletons of
the swa mp ghost crab, Ucides co rda /u s (Linn aeus),
ca n remove and concentrate go ld from ani oni c go ld
cya nide so luti ons over a wide range of pH values:10
The max imum AuCN ; uptake occurred at pH 3.7,
co rres pondin g to a fin al va lue of 4.9 g Au/k g OW ;
exoskeletons burnt in a non-oxid izing atmosphere
removed 90% of th e go ld at pH 10. phenolic gro ups
created durin g th e hea t treatment seemed to be the
main functional group respons ibl e for AueN ;
3o
bind ing by burnt ac id-washed crab shells .
Bioconcentrati on factors (BCFs) we re reco rded for
ca rrier-free 19X Au+ (ph ys ical half-life of 2.7 days) in
fres hwater orga ni sms after immersion for 2 1 days in a
med ium co nt aining 25,000 pCiIl =675 ,700 Bq1l 32 . In
goldfi sh, Ca rassills a llra/us (Linnaeus), th e hi ghes t
BCFs meas ured were < I in mu cle (i.e., less th an
675.700 Bq/kg FW musc le), 10 in viscera, and 9 in
who le fish. In th e freshwater winged tloater clam,
Anodonw /lIm a/liana Lea, th e maximum BCF was 7
in soft parts; for crayfish (A slacus sp. ), BCFs were < I
ill mu scle and 14 in viscera. For marin e organ isms
immersed for 26 days in sy ntheti c seawater cont ainin g
33.000 pCi/1= 89 1,900 Bqi l. max imum BCFs
meas ured we re tl in musc le and 16 in visce ra of th e
red crab . Ca llce r produ c/ll s Rand all , 11 in so ft parts
of the buller ciJ m, Saxidol1l11s gigan /ells (Deshayes),
12 in soft parts of the co mmon mussel, MYlilus edlllis
Linnae us, and < I in muscle and I in a whole gobiid
fish. th e longjaw mudsucker, C illiclilhys l1Iimbilis
Coope1}2. Max imum stabl e go ld concentrati ons
recorded in soft ti ssues of marine molluscs and
crustaceans ranged from 0.3 to 38.0 J1. g Au/kg OW ;
for fish musc le, the mean concentrati ons were O. I
J1. g/k g OW and 2.6 J1.g/kg ash weight 35 . In studi es with
th e eastern oyster, C rassos/rea virgill ica (Gmelin ),
the blue crab, Callinectes sapidus Rat hbun , and th e
mummichog Fundulus hele roclitus (Linnaeus), an
estu arine cyprinodon tiform fi sh, all species were
exposed in cages under field conditi ons to sediment-
sorbed, carrier-free, 198 Au + :14. The max imum level of
rad iogo ld in the caged organi sms was detected in
oysters 17 hr after contact with 198A u-spiked sed iments.
Indi ge nous orga ni sms collected 4 1 hr after contact
with the 198 Au-labeled sed iments contai ned no detec table
4
rad ioactivit/ . In a 25-day study with blue crab,
north ern quahog clam Mercenaria mercenaria
(Linnaeus), and the sheepshead minnow Cyprinodon
variegatus Lacepede, all species were maintained in a
1000-1 aquarium containing bentonite clay and seawater
spiked with carrier-free 199 Au (phys ical half-life of 3.2
days), as AuCi ); crabs accumul ated the most radi oacti vi-
ty, followed by clams, clay, and fi sh, in that o rd er:l~ .
Bioconcentration factors (BCF's) for metal s and
aq uatic orga ni sms deriv ed from carrier-free radio-
tracers in th e medium are probably artificiall y hi gh,
and should be interpreted with ca uti on 35 .36. For metals
it is a general observati on that high BCF's are
associated with low co ncentrations in th e medium.
and th at BCF's are especiall y hi gh when they are
derived from carrier-free radioi sotopes. Typicall y,
BCF's for metals and other chemicals studi ed reach a
plateau before declining with increasing concent ra-
ti ons in solution35 .36 . The maximum co ncentration of
stable go ld meas ured in ti ss ues of living marine
orga ni sms was 38.0 J1.g/k g FW35.
Conclusion
Gold recovery by selected species of bacteria, algae,
fun gi, yeasts, and hi gher plants from dilute solutions
under contro lled phys icochemical conditi ons seems
eco nomica ll y viable, with concentrat ion: up to 100 g
Au/kg OW documented . Dried crab exos keletons also
show promise for commercial go ld recovery from
solut ion (4.9 g Au/kg OW); however. go ld uptake by
li ving species of aq uati c macrofauna see ms negligible.
The mechani sms of accumul at ion wh ich include
ox idation, reduction, dissoluti on, leac hin g and sorption
are not knovin with certainty and merit additiona l
resea rch effo rt .
Acknowledgement
The author th ank s Drs. Peter H. Albers and Barnett
A. Rattner for th eir cons tru cti ve co mments on an
ea rl y draft.
 EISLER: BIORECOVER Y OF GOLD
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