Journal of Microbiological Methods 8 (1988) 5 1 - 9 0 51

El s e v i e r
J MM 00256
Preparati on and appl i cat i ons o f i mmobi l i zed
mi croorgani sms: a survey of recent reports
Mi c h a e l P. Co u g h l a n a a n d Ma r e k P.J. Ki e r s t a n b
aDepartment of Biochemistry, University College, Galway (Ireland) and bDalgety PLC, Group
Research Laboratory, Station Road, Cambridge, CB1 2JN (England)
( Re c e i ve d 25 No v e mb e r 1987) ( Ac c e p t e d 14 J a n u a r y 1988)
Contents
I n t r o d u c t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51
Revi ews . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
I mmo b i l i z a t i o n a n d i mmo b i l i z e d p r e p a r a t i o n s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52
Re a c t o r s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
Ap p l i c a t i o n s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
Ami n o a c i ds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
An t i b i o t i c s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
Bi o ma s s c o n v e r s i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
E t h a n o l a n d o t h e r s o l v e n t s o r f ue l s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
Food, d a i r y a n d d r i n k s i n d u s t r i e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Or g a n i c a c i d s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
Pr o t e i n p r o d u c t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
St e r o i d t r a n s f o r ma t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
E n v i r o n me n t a l d e c o n t a mi n a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
Ni t r o g e n f i x a t i o n . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
Mi s c e l l a n e o u s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62
P r o s p e c t s f or t h e f u t u r e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
Ac k n o wl e d g e me n t s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
Re f e r e nc e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
Introduction
I n t he pr ef ace t o his book on i mmobi l i zed bi ocat al yst s, Chi bat a [1] st at ed t hat
while enzymes are pr oduced by all living t hi ngs t hose f r om mi cr obi al sources are t he
mos t sui t abl e for i ndust ri al pur poses. Pr oduct i on of such enzymes is not l i mi t ed by
l ocat i on or season and cost s are low. Fur t her mor e, t he t i me requi red for pr oduct i on
Co r r e s p o n d e n c e t o: Mi c h a e l P. Co u g h l a n , De p a r t me n t o f Bi o c h e mi s t r y , Un i v e r s i t y Col l e ge , Ga l wa y,
I r e l a n d .
0 1 6 7 - 7 0 1 2 / 8 8 / $ 3. 50 1988 El s e v i e r Sc i e nc e P u b l i s h e r s B.V. ( Bi o me d i c a l Di v i s i o n )
52
is qui t e short and scale-up is possible. However, mi crobi al enzymes, like t hose f r om
ot her sources, when isolated f r om t hei r nat ural envi r onment are generally unst abl e
and are easily denat ur ed under operat i ng condi t i ons. Moreover, t hei r use is restricted
in t he mai n t o t he catalysis of single react i ons in whi ch cof act or regenerat i on is not
required. These probl ems may be obviated, or at least mi ni mi zed, by direct
i mmobi l i zat i on of mi crobi al cells cont ai ni ng t he desired activity or activities [2].
Operat i ng costs are lowered si gni fi cant l y because enzyme ext ract i on and pur i f i cat i on
is no l onger necessary and because hi gher yields of activity are obt ai ned on
i mmobi l i zi ng cells r at her t han free enzymes [2]. I mmobi l i zed viable cell systems also
have advant ages over t radi t i onal bat ch ferment at i ons. These include hi gher pr oduct
yields, t he ability t o operat e cont i nuousl y and at high di l ut i on rates wi t hout cul t ure
washout , t he capaci t y t o recharge t he system by i nduci ng growth of resting cells, and
accel erat ed react i on rates because of increased cell densi t y [2].
The first successful i ndust ri al appl i cat i on of i mmobi l i zed mi crobi al cell
preparat i ons, i.e., t he cont i nuous pr oduct i on of l : aspart i c acid, was carri ed out by
Chi bat a and colleagues in 1973 [1]. In t he intervening years t he number of report s
and pat ent s on t he uses of i mmobi l i zed mi croorgani sms has mus hr oomed despite t he
fact t hat restricted permeabi l i t y of cell walls to substrate and pr oduct and t he
occur r ence of unwant ed si de-react i ons cont i nue to pose problems. In our survey of
t he literature f r om J anuar y 1983 to Oct ober 1987 we f ound t hat mor e t han 600
papers on t he pr epar at i on and appl i cat i ons (excluding anal yt i cal uses) of
i mmobi l i zed mi croorgani sms have been published. Anal yt i cal uses of such
preparat i ons are deal t with in detail elsewhere in this vol ume [3].
Reviews
The impressive number of review articles on t he pr epar at i on and appl i cat i ons of
i mmobi l i zed mi croorgani sms t hat have been publ i shed since 1983 obvi ousl y reflects
t he consi derabl e research ef f or t and general interest in this topic. Such reviews
i ncl ude t hose of a general nat ure [2, 4 - 39] and it is perhaps fitting t hat among these
is a historical t r eat ment of t he subject by Chi bat a and colleagues [11]. The most
recent general review, t hat by Aki n [39], covers such topics as advant ages and
di sadvant ages of i mmobi l i zed cells, suppor t s and i mmobi l i zat i on procedures used,
and appl i cat i ons and per f or mance characteristics of i mmobi l i zed cell biocatalysts.
Ot her reviews concent r at e on suppor t s or procedures for i mmobi l i zat i on [ 40- 46], on
vari ous aspects of process engi neeri ng [ 47- 54] , on t he design and per f or mance of
react ors [ 55- 57] and on t he probl ems of ensuri ng an adequat e suppl y of oxygen t o
t he i mmobi l i zed cells duri ng oper at i on etc. [58].
Immobilization and immobilized preparations
I mmobi l i zed cell bi ocat al yst s may be def i ned as cells t hat are physically restricted
t o a def i ned space with ret ent i on of some or all of t hei r cat al yt i c activity for repeat ed
and cont i nuous use (see, e.g., Ref. 39). One may add t hat i mmobi l i zat i on is also
desi gned t o make t he cell catalysts mor e amenabl e t o handl i ng and cont rol . Among
t he procedures used t o i mmobi l i ze mi croorgani sms are aggregat i on or fl occul at i on,
53
adhesi on or adsorpt i on, covalent linkage of cell to cell or cell to support, ent rapment
or encapsul at i on in gels or ot her polymers, and physical retention wi t hi n
membr anous structures or hollow fibres. Examples of each of these procedures for
i mmobi l i zat i on and descriptions of new support s have been the specific subject
mat t er of a large number of papers [59-110]. As stated above, the object of
i mmobi l i zat i on is to restrict cell mi grat i on with mi ni mal i nhi bi t i on of catalytic
capacity. However, it must be said t hat in many systems the condi t i ons used in
i mmobi l i zat i on and the resultant highly localized concent rat i on of cells have been
seen to affect growth and mor phol ogy [111-117]. The effects of i mmobi l i zat i on on
general met abol i sm or specific enzyme activities [51, 118-132] have also received the
at t ent i on these aspects deserve. Any immobilized microbial preparat i on dest i ned for
serious appl i cat i on must, among ot her qualities, be stable in operation. In this context
several papers [133-139] specifically devoted to stability, stabilization and activation
are of interest, as are those [140-146] detailing procedures for exami nat i on of immobil-
ized preparations.
The most commonl y used met hod of cell i mmobi l i zat i on has been ent rapment or
ecapsul at i on in gels and polymers, bot h nat ural and synthetic. Hydrocol l oi d gels,
especially alginates, cont i nue to be the favourite support al t hough with a range of
variations from the original procedure [99, 137, 147]. Alginic acid is a pol ymer of
D-mannuroni c and L-guluronic acids j oi ned by ~-1,4 and o~-1,4 glycosidic linkages.
Solutions of sodi um alginate are viscous. By contrast, calcium alginates are gels, the
calcium ions acting as bridges between pol ymer chains at guluronic acid residues. As
stated above, alginates are among the more favoured supports because t hey are
nont oxi c and because the ease with which gel f or mat i on takes place allows mild
condi t i ons to prevail duri ng i mmobi l i zat i on. In essence i mmobi l i zat i on is effected by
suspendi ng cells in a sol ut i on of sodi um alginate which is t hen dropped, extruded
or sprayed i nt o a sol ut i on cont ai ni ng calcium [46]. The gel beads t hat form are
usual l y allowed to harden for a peri od in which calcium cross-linking is maximized.
While it is possible to use a range of ot her divalent ions for gel format i on, calcium
is generally considered to be the most appropriate. The ent rapped cells have an
element of freedom wi t hi n the gel structure and can multiply. However, growth at
or near the surface may result in loss of cells, with consequent det eri orat i on of
catalytic ability and cont ami nat i on of the subst rat e/ product stream in use.
Denat ur at i on of the bead structure can occur as a result of compet i t i on with other
ions for bi ndi ng sites and i f calcium is removed by precipitation with phosphate. It
is typical in the practical usage of al gi nat e-ent rapped mi croorgani sms to mix cells
(ranging in concent rat i on from 10- 30 g/100 ml) with an equal vol ume of sodi um
aiginate (4o70, w/v) so t hat a final bead concent rat i on of 27o (w/v) is achieved [46,
148-153]. In l aborat ory-scal e t echnol ogy beads may conveniently be formed by
dropwise addi t i on of the cel l / sodi um alginate mixture from a syringe into the
calcium chloride solution. This can of course be mechani sed and bead size may be
altered by j udi ci ous choice of the bore size of the syringe needle. Bead shape may also
be altered to suit the i nt ended appl i cat i on [99]. Moreover, it has recently been
report ed t hat t he use of resonance techniques to break up the j et of
bi ocat al yst / al gi nat e mixture into droplets of uni f or m size as t hey are i nt roduced into
the divalent cat i on sol ut i on increases by two orders of magni t ude the scale of
54
i mmobi l i zat i on over t hat whi ch can be achieved by convent i onal nozzl e i nj ect i on
[153I.
Apar t f r om alginates, t he most commonl y favoured hydrogel for cell
i mmobi l i zat i on is carrageenan. Its st ruct ure is similar to t hat of agar. It is
gal act opyr anosyl - based with a si gni fi cant percent age of subst i t ut ed residues. It is
compr i sed of a number of maj or fract i ons of whi ch t he K, t he most f r equent l y used,
and t fract i ons f or m t hermoreversi bl e gels. Gel st ruct ures are achieved by f or mat i on
of i nt erchai n helices. On warmi ng t o 50C, 5% (w/v) K-carrageenan exists as a
sol ut i on in whi ch t he pol ymer chai ns are present as r andom coils. To maxi mi ze gel
per f or mance, t he car r ageenan can be washed with 3% (w/v) sucrose t o remove
cal ci um ions. The car r ageenan sol ut i on is t hen mi xed with an equal or less t han
equal vol ume of cells and t he mi xt ure is dr opped i nt o a col d sol ut i on of ei t her KCI
or CaC12. Beads f or med on cool i ng using CaCI2 are t hen har dened or cured using
KCI. Ultimately, pot assi um is used as t he stabilizing cat i on. The t emper at ur e of t he
cel l / car r ageenan sol ut i on used is critical in t hat it det ermi nes t he effi ci ency of bead
f or mat i on and may have an adverse affect on cell viability. Nevertheless, t he
st ruct ural i nt egri t y of a gel so f or med is not as sensitive as t hose f or med f r om
alginates t o t he presence of ani ons and cat i ons in t he macr oenvi r onment [98].
Modi f i ed procedures, e.g., t he i ncl usi on of silica, have been investigated [51, 149].
For mat i on of beads by suspensi on of t he monome r in hydr ophobi c phases is also
showing promi se [43, 104, 1571. Pr epol ymer i zed synt het i c mat eri al s have also been
used as ent r appi ng or encapsul at i ng medi a [72, 100, 154] as have a range of
mi scel l aneous nat ural gels i ncl udi ng agar [361, chi t osan [67, 133, 155], col l agen [39,
77, 156], egg white [101], gelatin [391, l ocust bean gum [158], vari ous mixed gel
systems [39, 102, 1581 and mat eri al s t hat can be copol ymer i zed by r adi at i on [59, 61,
69, 71, 1031. Ot her mat ri ces are i ncl uded in t he reference list [59, 110]. Celite has been
i ncl uded in some ent r apped bi ocat al yst systems t o i mprove on gel permeabi l i t y and
robust ness [391.
A mor e pragmat i c appr oach t o i mmobi l i zat i on of bi ocat al yst s is t o encour age t he
growt h of cells in voids in por ous materials. The success of such systems derives f r om
t he nat ural t endency of mi crobi al cells t o adhere t o surfaces ( adsor pt i on) or t o one
anot her (fl occul at i on). In a t ypi cal exampl e yeast cells have been i mmobi l i zed in
1 cm 3 ret i cul at ed pol yur et hane cubes by growing t he cells in cont act with t he
suppor t f or 20 h [1591. The cubes can t hen be packed in col umns or used in t ower
f er ment er systems. Such catalysts do not suffer t he di sadvant age of alginate beads
in bei ng sensitive t o t he presence of ani ons and cat i ons t hat mi ght di srupt t hei r
st ruct ural i nt egri t y nor are t he cells subj ect ed t o possible heat shock denat ur at i on
as coul d be t he case in t he pr epar at i on of car r ageenan systems. They do not , however,
af f or d t he same degree of cont r ol over cont ami nat i on of pr oduct streams. Various
cloths, foams, sponges and metallic meshes have been used as i mmobi l i zat i on
support s. Since t hese are usual l y bot h robust and inexpensive, scale-up of such
systems is relatively easy [115, 124, 160-1631. Moreover, t he processes of
i mmobi l i zat i on are general l y qui t e simple. As an exampl e we may cite t he
i mmobi l i zat i on of Erwi ni a on DEAE- cel l ul ose whi ch is achieved merel y by mixing
cells with a sl urry of t he resin (2 g cells/10 ml resin) at pH 7 [152]. Thi s pr ocedur e
is anal ogous t o i mmobi l i zat i on of prot ei ns by i oni c binding. In general, i mmobi l i zed
55
cell systems depend not only on physical entrapment factors resulting from colony
growth but also on a variety of adhesion forces. The latter may be enhanced in
porous or non-porous support matrices by any one of a variety of possible
modifications to the cells or to the supports [42, 44, 75, 78, 105, 106, 164-166]. One
such modification involves the adsorption of aluminium ions onto the surface of
Saccharomyces cerevisiae [75, 167, 168]. The aluminium ions neutralize repulsive
charges and so facilitate adhesion of the cells to glass plates.
Aggregation and flocculation, a form of cell immobilization, is frequently used to
exploit the catalytic abilities of certain microorganisms in established tower
fermenters. Various examples of systems operated in this mode have been reported
[169-171]. Flocculation may be stimulated or enhanced by the use of
polyelectrolytes, various gas treatment techniques or by covalent bonding [172, 173].
One example is the cross-linking of permeabilized yeast cells using albumin and
glutaraldehyde [109]. A disadvantage of this system and those like it is that the
bifunctional reagent used in cross-linking, by reacting with essential cellular
components, may effect significant loss of catalytic activity.
Various membrane systems not only provide a means of immobilizing cells they
also provide the reactor vessel. Such systems may however experience problems as
a result of excessive cell growth and biomass build-up [174]. A typical example of
the use to which such systems may be put is the immobilization of yeast cells within
ultrafiltration hollow fibres [175]. The fibres used had a nominal molecular weight
cut-off value of 10000 and to prevent the build-up of biomass a nitrogen-deficient
medium was used.
Reactors
In theory, immobilized cell catalysts may be used in stirred-tank reactors. In
practice, however, this mode of operation has not been favoured. Membrane systems
including ultrafiltration cells and hollow fibre reactors have enjoyed considerable use
as have those dictated by specific requirements, e.g., in biosensors [107, 174, 176,
177]. However, a survey of the literature shows that two major systems, plug-flow
and air-lift bioreactors, continue to predominate [36, 39]. A problem associated with
bioreactors destined for use with living cells is that of gas production. In the packed-
bed type, gas generation leads to the development of considerable pressures on the
reactor walls. In the case of air-lift types, the accumulation of gases within beads
necessitates the incorporation of limiting mesh systems that prevent the loss of beads
from the top of the reactor. In attempts to overcome these problems a bioreactor
system consisting of cascades of fluidized-beds with side loops for aeration and
stripping of carbon dioxide has been devised [51]. An alternative approach involves
the introduction of a basket containing immobilized cells into an appropriate vessel
so as to create a bioreactor. Such a system has been investigated for the continuous
acidification of milk and for the production of ethanol [150, 178]. Further variations
have included the use of rotating biological surface reactors [179-181] and the use
of film fermenters. In one such fermenter cotton cloth provides the support [172].
Immobilization of microorganisms and incorporation of the preparation into a
reactor creates a complex dynamic situation in which the potential for cell growth
56
and the diffusion of gases, substrates and products must be considered. Reactor
design and the problems associated with mass transfer of substrates and products
have been the subject of a number of papers and review articles [48, 51, 55, 108, 110,
114, 118, 133, 143, 163, 182-206]. Other papers have dealt with procedures for
ensuring an adequate rate of oxygenation during operation [207-210].
Applications
Current applications of immobilized microorganisms on an industrial-scale are,
with few exceptions, restricted to the production of antibiotics, amino acids and
organic acids. Nevertheless, research in many different countries shows that the
potential of these preparations for other applications is enormous. Thus, apart from
the above, they may find use in the production of ethanol and other fuels, in the
exploitation of biomass, in organic syntheses, in wastewater treatment and in the
food, dairy and drinks industries. Current and potential applications have been well
reviewed [132, 154, 211-221]. In the text to follow, we have tried to sort into related
groups the papers dealing with specific uses of immobilized microorganisms. Howev-
er, strict categorization is not possible. For example, immobilization of an organism
with a view to producing cellulase could be included under protein synthesis or
biomass exploitation. Similarly, biomethanation of organic nutrients in aqueous
effluents could be listed under wastewater treatment or fuel production. Despite this
we trust that the reader will readily be able to locate the references of interest.
A m i n o aci ds
The production of amino acids, is, as stated earlier, one of the most successful
applications of immobilized microbial cells [26]. Procedures for the formation of
amino acids generally from ketoacids [222] and for the specific production of alanine
[223-229], arginine [230], aspartate [231-244], glutamate [245], N-acetyl
methionine [246], phenylalanine [247-250], tryptophan [251] and tyrosine
[252-256] have also been reported. Chibata and co-workers at the Tanabe Seiyaku
Co. in Osaka have developed a process whereby asparate and alanine can be
produced from ammonium fumarate by sequential exploitation of the aspartase
activity of immobilized E. col i and the aspartate decarboxylase activity of
immobilized P d a c u n h a e [223-225]. The 1984 production rates of alanine and
aspartate were 10 tonnes/month and 100 tonnes/month, respectively [223]. The
operational stability of the cellular aspartase (T,/2 4 months), by contrast with the
instability of the free enzyme, and the use of mutants of E. col i lacking fumarase
activity (thereby eliminating the conversion of fumarate to malate) contributed
significantly to these impressive production figures [235]. The interfering fumarase
(E. col t ) and alanine racemase (P.. dac unhae ) activities could also be selectively
eliminated by appropriate treatment of the cells prior to immobilization [218]. The
Wu-Sxi Solvent Factory in China and Kyowa Hakko Kogyo Co., Ltd. in Japan also
produce aspartate using a similar procedure [150]. Evans and colleagues [250] have
recently reported the isolation of a strain of Cor y ne bac t e r i um e qui that produces
more than 33 g/l of L-phenylalanine from c~-acetamidocinnamic acid (ACA) in molar
yields greater than 997o using immobilized cells. The inducible cellular activities
57
ACA translocase
Acetamidocinnamate (exogenous) ~ Acetamidocinnamate (endogenous)
ACA acylase II
Phenylpyruvate ~ ~
NH4+ I ~- ' " NADH
~ Phenylalanine dehydrogenase
~ "x,...__~ NAD +
L-Phenylalanine
a-Aminocinnamate
exploited in this process include a permease, an acylase and a dehydrogenase.
An oxidizable substrate such as lactate, pyruvate or formate is included to ensure a
supply of NADH. A mutant, OARI-16, produces phenylalanine 2.5-times faster
than does the parent strain [250]. Moreover, it is insensitive to endproduct inhibition
and accumulates more than 30 g/1 of the amino acid. The authors discuss the
commercial feasibility of this system for the continuous production of L-
phenylalanine under mild conditions. Note than L-phenylalanine is important not
only as an essential amino acid in human nutrition but like asparate is also a raw
material for synthesis of the synthetic sweetener, aspartame. Thus, demand for the
amino acid is rising. One may also note that the feedstock containing a-
acetamidocinnamate, lactate and NH4OH is cheap and that reducing equivalents
are recycled by the sequential operation of lactate and phenylalanine
dehydrogenases. Nishida and co-workers [257] have also developed a procedure for
the production of L-phenylalanine from acetamidocinnamic acid using
coimmobilized cells of Corynebacterium sp. and Paracoccus denitrificans. This two-
step reaction (outlined below) is catalysed by the acetamidocinnamate
amidohydrolase activity of Corynebacterium sp. and the amino-transferase activity
of Paracoccus denitrificans [257].
Amidohydrolase Aminotransferase
Acetamidocinnamate
Phenylpyruvate f ~ L-Phenylalanine
+ L-amino acid
Antibiotics
The use of cell-free immobilized enzymes has had considerable impact on the
industrial production of antibiotics especially in those reactions involving only a
58
single step (see, e.g., Ref. 258). However, because of the "difficulties encountered
with complex total enzymic synthesis using such preparations" [258] it was perhaps
inevitable that the possible utility of immobilized whole cells in these processes
would receive attention. Indeed, several companies including Bayer and Beecham,
since 1969, and Taiyan Pharmaceutical and Shanghai Pharmaceutical, since 1978, have
had pilot plant if not industrial-scale facilities for 6-aminopenicillanic acid
production [218]. The potential of immobilized microorganisms in antibiotic
production has been reviewed by several investigators [258-262]. Specific reports
have also demonstrated that the total synthesis or modification of candidicin [263],
cephalosporins [264- 266], chlorotetracycline [267- 269], cyclosporin [270],
nikkomycin [271, 272], oxytetracycline [273], patulin [274-276], penicillin
[277-293], rifamycin [294-297], thienamycin [298-301] and tylosin [2721 by
immobilized whole cells is possible.
Bi omas s conversi on
Biomass may be defined as everything excluding fossil fuels that has been derived
as a result of photosynthesis. Whatever the definition used, biomass, whether
primary (trees account for 90%) or secondary (viz. wastes or residues of forest,
agricultural, domestic or industrial origin), is potentially a vast and renewable
reservoir of fuel and chemical feedstocks. Realization of this potential requires that
the major components of biomass, the polysaccharides cellulose and hemicellulose,
be degraded to their monomeric forms and sequentially or simultaneously fermented
to desired end products such as ethanol. The major bottleneck in achieving these goals
is the fact that cellulose, an insoluble crystalline material, is not very amenable to
hydrolysis. Thus, large amounts of cellulase are required for its conversion. To this
end various groups of investigators are actively searching for improved cellulase
producing organisms or are attempting by mutation or recombinant DNA
techniques to improve on the cellulase-producing abilities of known organisms or to
confer on non-cellulolytic species the ability to utilise this substrate. In the context
of the present survey we note that procedures for immobilization of Tri choderna
reesei, one of the most powerful cellulase-producing fungi, have been investigated
[302, 303] as has the ability of this and other organisms to produce cellulase when
immobilized [304-306]. Other reports deal with the ability of immobilized
cellulolytic organisms to saccharify cellulosic substrates [306-310] including sugar
cane bagasse [306], sawdust [309] and cereal chaff [310]. The hydrolysis of
cellobiose, a B-1,4-1inked dimer of glucose and the major endproduct of cellulase
action [311-313] and inulin, a polymer of fructose found, for example, in high yields
in Jerusalem artichoke [314, 315] by immobilized microorganisms exhibiting /3-
glucosidase and inulinase, respectively, has also been investigated. Anaerobic
digestion of 'wastes' such as pig slurry by immobilized consortia capable of
producing methane [316-318] may also be cited as examples of the use of
immobilized microorganisms in exploitation of the potential of biomass.
Et hanol and ot her sol vent s or f ue l s
Even a cursory perusal of the pertinent literature would show that the production
of ethanol is the most actively researched area of application of immobilized
59
microorganisms. Advances in this area were reviewed in 1984 by Margaritis and
Merchant [319] and more recently by Godia and colleagues [320]. Many papers and
patents relating to ethanol production deal with the organisms used, methods of
immobilization, as well as with process and reactor considerations [155, 164, 165,
169, 170-173, 175, 181, 321-396]. As further examples of the potential of biomass
as a source of fuels one notes that the possibility of using immobilized
microorganisms to produce ethanol from hydrolysates of wood [397], bagasse [398]
and other cellulosic raw materials [399] has been demonstrated as has that from
cellobiose [400-402], sucrose [403-405], apple juice [406], beet juice [407], cane
juice [147], molasses [408], sweet sorghum juice [409], banana fruit pulp sugar [410],
fructose [411], Jerusalem artichoke [412-415], starches [148, 159, 416-418], sugars,
such as xylose or xylulose, derived directly or indirectly from hemicellulose [191,402,
419-422] and from whey permeate or lactose [423-434].
The production of other solvents such as acetone and or butanol [151,435-444],
2,3-butanediol [445-448] and glycerol [449-452] and of gaseous fuels such as
methane [453-461] and hydrogen [193, 462-470] has also been examined. Two
papers deal with immobilized microorganisms as fuel cells [471, 472]. We may also
include in this section the report on the continuous transformation of benzaldehyde
to benzyl alcohol [177].
Food, dairy and drinks industries
The fermentative properties of microorganisms have long been used in the making
of those staples of life, bread, cheese, beer and wine. It is not surprising therefore
to find that much effort has been expended on examination of the possibility of
improving on the efficiency of some of these applications by using immobilized
microbial cells. For a review of advances in this area up to 1983 the reader is referred
to the paper by Weetall and Zelko [473]. Examples of specific applications of
immobilized cells include the reduction of the limonin and nomilin contents of citrus
juices so as to prevent the development of bitterness [474, 475]. However, the greatest
application of these preparations is in the production of high fructose syrups.
Approximately 6 million tons of high fructose syrup, representing 457o of the total
industrial sugar market, were produced in the U.S. in 1982 [218]. While it must be
said that the bulk of this was manufactured in processes using immobilized cell-free
glucose isomerase the use of immobilized whole cell enzyme is increasing. Indeed,
several companies including Gist Brocades, N.V. (Actinoplanes missouriensis),
Reynolds Tobacco Co. and ICI (Arthrobacter sp.), Novo Industri A/S (Bacillus
coagulans), Agency of Industrial Science and Technology (Streptomyces albus),
Miles Laboratories Inc. and Car-Mi (Streptomyces olivaceus), Denki Kogatsu Kogyo,
Nagase Sangyo and Nabisco Brands Inc. (Streptomyces sp.) currently produce high
fructose syrups using immobilized preparations of the named organisms [218]. The
process developed by Novo lndustri A/S in which pelleted cross-linked Bacillus
coagulans is the catalyst was, and perhaps still is, the most widely used commercially
[218]. In 1978 plants using this technology had a capacity of 2 million tonnes/year.
The majority of the reports during 1983-1987 on the use of immobilized
microorganisms for the production of high fructose syrups are concerned with
exploiting the glucose isomerase activity of the immobilized cells [476-482]. Howev-
60
er, several papers also deal with the inversion of sucrose by immobilized whole cell
invertase [483-486] or with the hydrolysis of inulin from Jerusalem artichoke
[487-490].
Isomaltulose, a natural component of honey, is a sugar of reduced cariogeneity
used in foodstuffs and pharmaceuticals. Its production using immobilized cells has
recently been investigated [152]. Indeed, in 1982 Tate & Lyle developed a pilot-scale
process for isomaltulose production using immobilized Erwinia rhapontici [218].
Sorbose, much of which is used in the synthesis of vitamin C, may be produced by
the oxidation of sorbitol using immobilized preparations of Gluconobacter
suboxydans or Acetobacter melanogenum [491-493]. Soy sauce, long produced by
traditional fermentation procedures, may also be prepared using immobilized cell
technology [494]. Osaki et al. using column type reactors containing various
immobilized microorganisms reduced the time taken for soy sauce production from
6 months to 2 weeks. However, it must be said that while the resultant sauce
resembled the real thing it had a quantitatively different pattern of organic acids and
aromatics than that enjoyed by the purists [494].
In the dairy industry immobilized microbial cells are also finding increasing use.
Examples include a glucose oxidase/E, coli coimmobilisate for the preservation of
milk [495], lactic acid production/prefermentation of milk for cheese making [178,
496-499], the production of yoghurt [500], Emmental [501] and Roquefort [502]
flavours and whey protein concentrates [503]. Immobilized microorganisms appear
to have great promise in brewing, i.e. in speeding up the time taken to make beer or
in improving the quality of the finished product [150, 504-514]. Other applications
include mead production [515, 516], wine-making, e.g. the production of sparkling
wines [517-519] and malolactic fermentation [520-524].
Organic acids
Several organic acids are important in the food, soft drink and pharmaceutical
industries and are essential intermediates in chemical syntheses [218]. Many of these
have been produced by traditional fermentation procedures. However, for others the
only economically feasible process is by the use of immobilized microorganisms. One
report, which again underscores the potential of biomass, details a procedure for the
production of organic acids by continuous fermentation of lignocellulosic substrates
[525]. Other papers provide details of processes for the production of acetic acid
[526-531], chorismic acid [532], citric acid [533-542], gluconic acid [543], itaconic
acid [544-547], lactic acid [548-552] and malic acid [553-556]. The latter is
produced on an industrial scale by the enzymic conversion of fumaric acid using
immobilized cells of Brevibacterium flavum [553]. The current process, patented by
the Tanabe Seiyaku Co. [554], is the result of a number of modifications designed
to improve on that first developed in the early 1970s. It is 21 times more efficient
than the original process and is capable of producing about 1 tonne of malic acid
per day from a 1000 litre column with 7007o of the maximum theoretical yield [553].
The historical development of this process has been related by Chibata and
colleagues [553]. The original process developed in 1974 utilised Brevibacterium
ammoniagenes with high fumarase activity immobilized in polyacrylamide gel. How-
ever, unconverted fumaric and succinic acids accumulated in considerable
61
quantities in the reaction mixture. The former could easily be precipitated by
acidification of the reaction mixture. However, separation of succinic and malic
acids is difficult. Fortunately it was found that pretreatment of the cells with bile
acids prior to immobilization significantly reduced the amount of succinic acid
produced. Moreover, such treatment increased the permeability of the cell
membranes to substrate and product so that the yield of malic acid was improved
considerably. The half-life of the fumarase activity of the immobilized cell column
under operating conditions was 53 days. However, the fumarase was partially
denatured during immobilization of the cells on polyacrylamide. A 5-fold
improvement in the process was subsequently made by changing from B.
ammoniagenes to B. flavum and by changing the support from polyacrylamide to
K-carrageenan. Subsequently, it was found that the addition of polyethyleneimine to
the immobilization medium increased the operational stability of the fumarase
activity in the immobilized preparation. The column could then be operated at
higher temperatures, 50-55 C, for long periods with the result that the current proc-
ess, in which unconsumed fumarate is recycled, is 21-fold more efficient than the
original [553].
Protein production
Most large-scale protein production processes involve either traditional liquid
cultivation or solid-state fermentation [218]. However, a number of investigators
have examined the possible potential of using immobilized microbial cells for these
purposes [176, 557-562]. Other reports since 1983 include the production of
cellulase by Trichoderma reesei [302-305] or by Sporotrichum cellulophilum [306],
amylases [563 -565], chlorperoxidase [566], lipase [567] and proteases [568, 569]. An
immobilized rDNA E. coli system was claimed to produce '407o pure' ~3-1actamase
for several months without significant loss of activity [194, 570]. One presumes that
this means that t3-1actamase accounted for 407o of the total protein produced by the
system during operation.
Steroid transformation
Transformation of steroids has in the past been carried out by conventional fer-
mentation procedures because of the difficulties involved in chemical transformati-
on [218]. The possibility of using immobilized cell-free enzymes is impractical since
the more important steroid-transforming enzymes, dehydrogenases and hydroxyla-
ses are highly labile and difficult to obtain in quantity [571]. Furthermore, many
of the desired transformations involve multi-step reactions in which cofactor rege-
neration is essential. For these reasons steroid transformation using immobilized mi-
crobial cells is becoming the state-of-the-art. Indeed, the first such transformation
was carried out in 1970 [571]. In their excellent review on the use of immobilized
cells in steroid transformation published in 1985, Koshcheyenko and Sukhodolskaya
[571 ] discussed the more important enzyme and multienzyme reactions involved and
gave details of the procedure for immobilization and utilisation of the appropriate
microorganisms. Since 1983 several papers on this subject have been published. These
include descriptions of immobilization procedures, reactors or processes [572-576]
and those on applications [577- 599] including ALdehydrogenation [167,585- 590],
62
1 lo~-hydroxylation [591 -593], 16e~-hydroxylation [594, 595], 17~-hydroxylation [596,
597] and sequential reactions involved in the synthesis of prednisolone from cortexo-
lone [598].
Environmental decontamination
Environmental decontamination is one area in which immobilized microorganisms
already have application. Indeed, one aspect of this topic, i.e., wastewater treatment,
is currently the major large-scale application of surface-bound microbial cells [218].
For example, the Norton Co. in Oak Ridge, TN, have since 1976 operated a large-
scale wastewater treatment unit involving microorganisms adsorbed on anthracite
in a tapered up-flow anaerobic bioreactor [218]. Advances in the aerobic and anae-
robic treatment of wastewaters, effluents and condensates using immobilized whole
cells have been reviewed by several investigators [179, 184, 186, 187,600- 609]. Pro-
cesses for removal/recovery of heavy metals have been documented [610-617] as
have those for removal of phenols [618- 624], chlorinated phenols, benzoates and
hydrocarbons [625 -629]. Procedures for nitrification and denitrification [163, 172,
630- 633] and for the elimination of cyanide [634], triazine [635], ammonium and
phosphate ions [636] and hydrogen sulphide [637] have also been reported. Dehy-
droabietic acid, a component of many pulp mill effluents, is toxic to fish. However,
it can be converted to harmless products using mycelia of Mortierella isabellina free
or entrapped in alginate [638]. Entrapment stabilized the hydroxylase activity invol-
ved in detoxication. A procedure, based on the use of immobilized Pseudomonas
indigofera, has been developed for the degradation of anabasine, an insecticide con-
taminating soils [639]. MacRae [640] has demonstrated the potential of using Rho-
dosphaeromonas sphaeroides or Alcaligenes eutrophus adsorbed to magnetite for the
removal of the pesticides lindane, 2,4-dichlorophenoxy acetic acid (2,4-D) and
2,4,5-trichlorophenoxy acetic acid (2,4,5-T) from contaminated waters.
Nitrogen fixation
The possibility of using alginate beads as inoculant carriers for the slow release
of bacteria that affect plant growth is under investigation [641]. Immobilized prepa-
rations capable of fixing nitrogen [642] and of photoproducing ammonia [643,644]
have also been subjects of recent research.
Miscellaneous
Included in this section are procedures for the production of acrylamide [645 - 648]
alkaloid synthesis or metabolism [649- 652], conversion of alkenes to epoxides [149,
653 - 656], synthesis of 3,4-dihydroxyphenylalanine [DOPA; 657 - 661], synthesis or
conversion of lipids or lipid-soluble materials [662 - 666], NAD regeneration [ 192,
667, 668] and selective reduction of oxo acid esters [669, 670]. Other papers provide
details of processes for the production of cyclopropane carboxylic acids [671], hy-
drocarbons [672], anthraquinone [673], 2-keto-3-deoxygluconate [674], polysaccha-
ride [675], pigment [676], gibberellic acid [677], glutathione [678], water-soluble
compounds [679], cytidine diphosphocholine [156] and vitamins [680, 681]. Several
other transformation or conversion reactions catalysed by immobilized cells have also
been reported. These include hydroxylation of indolyl-3-acetic acid [682], conversi-
63
on of chenodeoxycholic to ursodeoxycholic acid [683], conversion of dihydrouracil
to uracil [684], stereospecific hydrolysis of d-I-menthyl acetate [685], cathecol syn-
thesis from benzene [686], degradation of n-valeric acid [687], depolymerization of
chondroitin C sulphate [688], reduction of nitro derivatives of 1,2-dihydro-3H-1,4-
benzodiazepin-2-ones [689], oxidation of secondary alcohols to methyl ketones [690],
reduction of terpenic ketones [691] and the preparation of peptides [692].
Prospects for the future
Immobilized cell technology is already established in certain areas such as amino
acid production. The techniques of immobilization and of reactor design and utilisa-
tion have been well documented in many hundreds of review articles and research
papers. This should encourage those who wish to produce specialized materials for
which no alternative route is available as well as those who see possibilities for im-
provement on traditional fermentation methods. Most reviewers are agreed that re-
s e a r c h i n t h i s a r e a wi l l c o n t i n u e a p a c e a n d t h a t r e c o mb i n a n t DNA p r o c e d u r e s c o u p l e d
wi t h t h e i mmo b i l i z a t i o n o f mi c r o b i a l , p l a n t a n d a n i ma l c e l l s wi l l a d d a n e w d i me n s i -
o n t o a f i e l d t h a t a l r e a d y s h o ws g r e a t p o t e n t i a l .
Acknowledgements
Our thanks to Roger Fensom and Carmel O'Sullivan for their expert assistance.
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573 Borman, E. A. and Turkina, M.V. (1983) Studies on the preculiarities of the immobilization and
transformation of sterols by cells of Mycobacterium phlei 1026 incorporated into polyacrylamide
gel. Appl. Biochem. Microbiol. 19, 284-289.
574 Manecke, G. and Klussmann, U. (1985) Immobilization of Corynebacterium simplex by inclusion
in synthetic cross-linked gels as biocatalysts for transformation of steroids. Angew. Makromol. Chem.
134, 125- 149.
575 Kloosterman, J. IV and Lilly, M.D. (1985) An airlift loop reactor for the transformation of ste-
roids by immobilized cells. Biotechnol. Lett. 7, 25- 30.
576 Flygare, S. and Larsson, P.-O. (1987) Steroid transformation using magnetically immobilized My-
cobacterium sp. Enzyme Microb. Technol. 9, 494-499.
577 Kloosterman, J. IV and Lilly, M.D. (1986) Pilot-plant production of prednisolone using calcium
alginate-immobilized Arthrobacter simplex. Biotechnol. Bioeng. 28, 1390- 1395
578 Yu, D., Zhou, P., Niu, J., Liu, S. and Chu, Z. (1984) Immobilized cells of Rhizopus nigricans and
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579 Yang, L. and Zhong, L. (1984) Transformation of steroids by immobilized microbial ceils. Ann.
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580 Yang, L. and Zhong, L. (1984) Transformation of hydrocortisone by immobilized Arthrobacter
simplex. Wei Sheng Wu Hsueh T' ung Pao, 11, 149- 150.
581 Borman, E. A., Koshcheenko, K. A. , Vinokurova, N. G. and Romanova, I.B. (1985) Microbiologi-
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cal hydrolysis of steroid ethers by Arthrobacter citreus VKM 654. Prikl. Biokhim. Mikrobiol. 21 (4),
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582 Shen, Y. (1985) Technology for immobilization of living cells and its application in microbial trans-
formation of steroid hormones. Yiyao Gongye. 16(11), 514-519.
583 Rao, M.K., Madyastha, K.M. and Bhattacharyya, P. K. (1986) Sterol side-chain cleavage by im-
mobilized Moraxella sp.: a continuous transformation. J. Microbiol. Biotechnol. 1(1), 7- 11.
584 Bihari, V., Joshi, A. K. , Jaiswal, R.C., Khan, A. W. and Basu, S.K. (1986) Use of fluidised bed
reactor for the transformation of steroids by immobilized cells. J. Microbiol. Biotechnol. 1(1), 41 -45.
585 Chert, K.C. and Hwang, K.R. (1986) Al-dehydrogenation of hydro-cortisone using immobilized
cells of Arthrobacter simplex. Chungkuo Nung Yeh Hua Hsueh Hui Chih. 24(1), 8- 14.
586 Yang, L. and Zhong, L. (1983) Preparation and properties of immobilized Arthrobacter simplex
BY-2-13 cells possessing 3-ketosteroid-Al-dehydrogenase activity. Wei Sheng Wu Hsueh Pao, 23,
128- 132.
587 Avramova, T. and Angelov, T. (1984) Immobilization of cells with steroid-l,2-dehydrogenase acti-
vity on different carriers. Acta Microbiol. Bulg. 14, 50-55.
588 Kloosterman, J., IV and Lilly, M.D. (1984) Effect of supersaturated aqueous hydrocortisone con-
centrations on the Al-dehydrogenase activity of free and immobilized Arthrobacter simplex. Enzy-
me Microb. Technol. 6, 113- 116.
589 Sonomoto, K., Matsuno, R., Tanaka, A. and Fujui, S. (1984) Kinetic study on Al-dehydrogenation
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590 Kloosterman, J., IV and Lilly, M.D. (1985) Maintenance and operational stability of immobilized
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377 - 382.
591 Broad, D. F. , Foulkes, J. and Dunnill, P. (1984) The uptake of Aspergillus ochraeus spores on dia-
tomaceous particles and their use in the 1 la-hydroxylation of progesterone. Biotechnol. Lett. 6,
357 - 362.
592 Bihari, V., Goswami, P. P., Rizvi, S. H. M., Khan, A. W. , Basu, S.K. and Vora, V.C. (1984) Stu-
dies on immobilized fungal spores for microbial transformation of steroids: 1 la-hydroxylation of
progesterone with immobilized spores of Aspergillus ochraeus G8 on polyacrylamide gel and other
matrices. Biotechnol. Bioeng. 26, 1403-1408.
593 Ceen, E. G. , Herrmann, J. P. R. and Dunnill, P. (1987) Solvent damage during immobilized cell
catalysis and its avoidance: studies on 11-c~-hydroxylation of progesterone by Aspergillus ochraeus.
Appl. Microbiol. Biotechnol. 25, 491-494.
594 Iida, M., Nakamura, T. and lizaka, H. (1983) Studies on microbial transformations. XI. 16c~-
hydroxylation of steroids with gel-entrapped Streptomyces roseochromogenes cells in water-organic
co-solvent system. Nippon Kagaku Kaishi, 9, 1393- 1399.
595 Chen, K.C. (1984) Steroidal 16a-hydroxylation using immobilized cells of Streptomyces roseochro-
mogenes. Chung Kuo Nung Yeh Hua Hsueh Hui Chih, 21, 30-38.
596 Turkina, M. V., Arinbasarova, A. Y. and Koshcheyenko, K.A. (1986) Entrapment of Saccharomy-
ces cerevisiae cells with 17~-hydroxysteroid dehydrogenase activity in polyacrylamide gel. Mikrobi-
ologiya, 55, 866-871.
597 Bihari, V., Joshi, A. K. , Khan, A. W. and Vora, V.C. (1985) Biotransformation of
3-methoxy-8,14-seco- 1,3,5(10),9(11)-estratetraen- 14,17-dione (Secodione) to its 17~-hydroxy deri-
vative (secol) using immobilized yeast cells (Pichia farinosa Y-118). Biotechnol. Bioeng. 27(9),
1347- 1352.
598 Mazumder, T.K., Sonomoto, K., Tanaka, A. and Fukui, S. (1985) Sequential conversion of cor-
texelone to prednisolone by immobilized mycelia of Curvularia lunata and immobilized cells ofA rth-
robacter simplex, Appl. Microbiol. Biotechnol. 21, 154-161.
599 Duarte, J. M. C. and Lilly, M.D. (1984) Cholesterol degradation by polymer-entrapped Nocardia
in organic solvents. Ann. N.Y. Acad. Sci. 434, 573-576.
600 Vogel, H. C. (Ed.) (1984) Advances in biochemical engineering/biotechnology. Vol. 29: Immobili-
zed biocatalysts; Saccharomyces yeasts; wastewater treatment. ISBN 3 540 12860.
601 Messing, R.A. (1983) Bioenergy production and pollution control with immobilized microbes. An-
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602 Shidara, S., Watanabe, A. and Suzuki, T. (1984) Studies on wastewater treatment by immobilized
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87
603 Cordoba, P. R. , Sanchez Piera, F. and Sineriz, F. (1984) Treatment of dairy industry wastewater
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604 Chevalier, P. and de la Noue, J. (1985) Wastewater nutrient removal with microalgae immobilized
in carrageenan. Enzyme Microb. Technol. 7(12), 621-624.
605 Aivasidis, A. and Wandrey, C. (1985) Anaerobic treatment of vapour condensates of the pulp in-
dustry with immobilized bacteria in a fixed bed loop reactor. Wiss. Umwelt. 1, 48- 57.
606 Gehring, H. (1985) Effluent treatment by the fixed-bed process. Chemicophysical and biochemical
process for cleaning organically contaminated industrial effluents with immobilized microorganisms
on carrier material. Melliand Textilber. 66(8), 591- 592.
607 Berkovitch, I. (1986) Cleaning up wastewater the Gist-Brocades way. Manuf. Chem. 57(3), 65 - 68.
608 Anon. (1986) A new anaerobic waste treatment process that resists toxic shock. Chem. Eng. (Int.
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609 Suzuki, T. (1986) Study of microorganisms used in wastewater treatment and bioreactors. Kankyo
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610 Anon. (1983) Immobilized bacteria mop up mine drainage. Biotechnol. Newswatch (McGraw-Hill),
3, 5.
611 Macaskie, L.E. and Dean, A. C. R. (1984) Heavy metal accumulation by immobilized cells of a Ci-
trobacter species. Biotechnol. Lett. 6, 71-76.
612 Macaskie, L.E. and Dean, A. C. R. (1984) Cadmium accumulation by immobilized cells of Citro-
bacter species. Environ. Technol. Lett. 5, 177-186.
613 Lancy, E.D. and Tuovinen, O. H. (1984) Ferrous ion oxidation by Thiobacillusferrooxidans im-
mobilized in calcium alginate. Appl. Microbiol. Biotechnol. 20, 94-99.
614 Anon. (1986) Algae show promise for metal recovery. Biotechnol. News. 5(23), 5.
615 Macaskie, L.E. and Dean, A. C. R. (1987) Use of immobilized biofilm of Citrobacter sp. for remo-
val of uranium and lead from aqueous flows. Enzyme Microb. Technol. 9, 2- 4.
616 Darnall, D.W., Greene, B., Hosea, M., McPherson, R.A. and Henzl, M. (1986) Recovery of hea-
vy metals by immobilized algae. Spec. Chem. R. Soc. Chem. 61, 1- 24.
617 Michel, L. J. , Macaskie, L.E. and Dean, A. C. R. (1986) Cadmium accumulation by immobilized
cells of a Citrobacter sp. using various phosphate donors. Biotechnol. Bioeng. 28, 1358- 1365.
618 Bettmann, H. and Rehm, H. J. (1984) Degradation of phenol by polymer entrapped microorganisms.
Appl. Microbiol. Biotechnol. 20, 285- 290.
619 Ehrhardt, H. M. and Rehm, H. J. (1985) Phenol degradation by microorganisms adsorbed on acti-
vated carbon. Appl. Microbiol. Biotechnol. 21, 32-36.
620 Anselmo, A. M. , Mateus, M., Cabral, J. M. S. and Novais, J. M. (1985) Degradation of phenol by
immobilized cells of Fusarium flocciferum. Biotechnol. Lett. 7(12), 889- 894.
621 Bettmann, H. and Rehm, H. J. (1986) Immobilized bacteria. Continuous degradation of phenol.
Chem. Ind. (Duesseldorf) 38(3), 278-280.
622 Dwyer, D. F. , Krumme, M. L. , Boyd, S.A. and Tiedje, J. M. (1986) Kinetics of phenol biodegrada-
tion by an immobilized methanogenic consortium. Appl. Environ. Microbiol. 52(2), 345 - 351.
623 Anon. (1986) Phenol solution detoxified biologically. Chem. Eng. News, 64, 16.
624 Fan, L. -S., Fujie, K., Long, T.-R. and Wang, W. -T. (1987) Characteristics of draft tube gas-liquid
fluidized-bed bioreactor with immobilized living cells for phenol degradation. Biotechnol. Bioeng.
30, 498 - 504.
625 Westmeier, F. and Rehm, H. J. (1985) Biodegradation of 4-chloro-phenol by entrapped Alcaligenes
sp. A 7-2. Appl. Microbiol. Biotechnol. 22(5), 301- 305.
626 Westmeier, F. and Rehm, H. J. (1986) Use of immobilization methods for biodegradation of chlo-
rinated phenols. Chem. Ind. (Duesseldorf) 38(3), 158-160.
627 Westmeier, F. and Rehm, H. J. (1987) Degradation of 4-chlorophenol in municipal wastewater by
adsorptive Alcaligenes sp. A 7-2. Appl. Microbiol. Biotechnol. 26, 78- 83.
628 Sahasrabudhe, S. R., Amin, A. R. and Modi, V.V. (1985) Transformation of chlorinated benzoates
and other benzene derivatives by Aspergillus niger and Aspergillusjaponicus. Appl. Microbiol. Bi-
otechnol. 21, 365- 367.
629 MacRae, I.C. (1986) Removal of chlorinated hydrocarbons from water and wastewater by bacteri-
al cells adsorbed to magnetite. Water Res. 20, 1149-1152.
630 Tramper, J. and Grootjen, D. R.J. (1986) Operating performance of Nitrobacter agilis immobili-
zed in carrageenan. Enzyme Microb. Technol. 8(8), 477-480.
88
631 Tramper, J. and de Man, A. W. A. (1986) Characterisation of Nitrobacter agilis immobilized in cal-
cium alginate. Enzyme Microb. Technol. 8(8), 472-476.
632 Tomizawa, K. (1986) Nitrogen removal using immobilized microbes. Gesuido Kyokaishi, 23, 57 - 66.
633 Kokufuta, E., Shimohashi, M. and Nakamura, I. (1986) Immobilization of Paracoccus denitrifi-
cans ceils with polyelectrolyte complex and denitrifying activity of the immobilized cells. J. Fer-
ment. Technol. 64, 533-538.
634 Zhou, X., Zhang, G., Cai, Z. and Gu, H. (1986) Cyanide degradation by immobilized cells of Fu-
sariurn sp. no. 12. Huanjing Kexue Xuebao, 6, 368-372.
635 Hogrefe, W., Grossenbacher, H., Cook, A. M. and Hutter, R. (1986) Biotreatment of s-triazine-
containing wastewater in a fluidized bed reactor. Biotechnol. Bioeng. 28, 1577- 1581.
636 Chevalier, P. and de la Noelle, J. (1985) Efficiency of immobilized hyperconcentrated algae for
ammonium and orthophosphate removal from wastewaters. Biotechnol. Lett. 7, 395-400.
637 Anon. (1987) Immobilized bacteria used to destroy noxious hydrogen sulphide gas. Biotechnol. Jpn.
Newsserv. 5, 6- 7.
638 Kutney, J. P. , Choi, L. S. L., Hewitt, G. M. , Salisbury, P. J. and Singh, M. (1985) Biotransformati-
on of dehydroabietic acid with resting cell suspensions and calcium-alginate-immobilized cells of
Mortierella isabellina. Appl. Environ. Microbiol. 49, 96- 100.
639 Aitkhozhina, N. A. , Dolobaeva, S.K. and Klyshev, L.K. (1986) Immobilization of the anabasine-
oxidising microorganism Pseudornonas indigofera. Prikl. Biokhim. Mikrobiol. 22(1), 49- 52.
640 MacRae, I.C. (1985) Removal of pesticides in water by microbial cells adsorbed to magnetite. Wa-
ter Res. 19, 825-830.
641 Bashan, Y. (1986) Alginate beads as synthetic inoculant carriers for slow release of bacteria that
affect plant growth. Appl. Environ. Microbiol. 51(5), 1089- 1098.
642 Murty, M. G. (1983) Immobilization of Beijerinckia, a nitrogen-fixing bacterium, on silica gel. Curr.
Sci. 52, 1031 - 1033.
643 Vincenzini, M., de Phillippis, R., Ena, A. and Florenzano, G. (1986) Ammonia photoproduction
by Cyanospira ri ppkae cells entrapped in a dialysis tube. Experientia, 42, 1040- 1043.
644 Jean-Fils, J. and Loudeche, R. (1986) Photoproduction of ammonia by immobilized heterocystic
cyanobacteria. Effect of nitrate and anaerobiosis. Biotechnol. Lett. 8(4), 265-270.
645 Yamaguchi, Y., Watanabe, I. and Satoh, Y. (1984) Process for the continuous production of acry-
lamide or methacrylamide using microorganisms. US Patent US 4, 440, 858.
646 Watanabe, I., Seki, S. and Ogawa, Y. (1985) Method for producing arcylamide using a microorga-
nism. European Patent Appl. EP 0150956, Pub. 7 Aug 1985. Appl. JP 7290/84, filed Jan 1984.
647 Hwang, J. S. and Chang, H. N. (1987) Continuous production of acrylamide by Brevibacteriurn sp.
immobilized in a dual hollow fibre bioreactor. Biotechnol. Lett. 26, 237- 242.
648 Maestracci, M., Bui, K., Thiery, A., Arnaud, A. and Galzy, P. (1984) A study of the inhibition
of an amidase with a wide substrate spectrum and its consequence for the bioconverion of nitriles.
Biotechnol. Lett. 6, 149-154.
649 Kopp, B. and Rehm, H. J. (1983) Alkaloid production by immobilized mycelia of Cl avi cepspurpu-
rea. Eur. J. Appl. Microbiol. Biotechnol. 18, 257-263.
650 Kopp, B. and Rehm, H. J. (1984) Semicontinuous cultivation of immobilized Claviceps purpurea.
Appl. Microbiol. Biotechnol. 19, 141- 145.
651 Furuya, T., Yoshikawa, T. and Taira, M. (1984) Biotransformation of codeinone to codeine by
immobilized cells of Papaver somniferurn. Phytochemistry, 23,999 - 1001.
652 Dmitrenko, G. N., Udod, V.M. and Gvozdyak, P. 1. (1985) Degradation of morpholine by immo-
bilized bacteria. Khim. Tekhnol. vody. 7(3), 71-73.
653 Hamstra, R.S., Murris, M.R. and Tramper, J. (1987) The influence of immobilization and redu-
ced water activity in gaseous-alkene oxidation by Mycobact eri um PY1 and Xant hobact er PY2 in
a gas-solid bioreactor. Biotechnol. Bioeng. 29, 884-891.
654 van der Meer, A. B. , Beenackers, A. A. C. M. and Stamhuis, E. J. (1986) Microbial production of
epoxides from alkenes in continuous multiphase reactors. Chem. Eng. Sci. 41(4), 607- 616.
655 Miyawaki, O.,Wingard, L.B. Jr., Brackin, J.S. and Silver, R.S. (1986) Formation of propylene
oxide by Nocardia corallina immobilized in liquid paraffin. Biotechnol. Bioeng. 28(3), 343 - 348.
656 Drozd, J. W. and Bailey, M.L. (1984) Biotransformation. European Patent Appl. EP 0, 099, 609.
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657 Wichers, H. J. , Malingre, T.M. and Huizing, H. J. (1983) The effect of some environmental fac-
89
tors on the product i on of L-DOPA by al gi nat e-ent rapped cells of Mucuna pruriens. Pl ant a, 158,
482 - 486.
658 Para, G. , Rifai, S. a nd Baratti, J. (1984) Pr oduct i on of L-DOPA from pyrocathecol and DL-serine
by bi oconversi on using immobilized Erwinia herbicola cells. Biotechnol. Lett. 6, 7 0 3 - 708.
659 Voivodov, K. I. , Tysyachnaya, I. V. , Gubni t ski i , L. S. , Yakovleva, V. I . and Berezin, I. V. (1985)
Enzymic synthesis of 3, 4-dihydroxyphenyl-z-alanine by free and immobilized cells of Citrobacter
f reundi i . Appl . Biochem. Microbiol. (Engl. Transl. ) 21(2), 127- 131.
660 Wichers, H. J . , Malingre, T. M. and Huizing, H. J . (1985) Opt i mi sat i on of t he bi ot r ansf or mat i on
of L-tyrosine i nt o L-dihydroxyphenylalanine (DOPA) by al gi nat e-ent rapped cells of Mucuna pru-
riens. Pl ant a. 166(3), 421- 428.
661 Voivodov, K. I. , Zueva, N. N. , Yakoleva, V. I. and Berezin, I. V. (1987) A kinetic study of t he syn-
thesis of 3, 4-dihydroxyphenylalanine by the Ci t robact erf reundi i cells immobilized in carrageenan.
Prikl. Biokhim. Mi krobi ol . 23, 192- 198.
662 Soda, K. (1983) Bioconversion of lipophilic compounds by immobilized biocatalysts in organic sol-
vents. Trends Biochem. Sci. 8, 428.
663 Tanaka, T. and Sonomot o, K. (1983) Fat -sol ubl e and sparingly water-soluble compounds in bio-
reactors. Saibo Kogaku, 2, 360- 368.
664 Wagner, F., Syldatk, C., Matulowic, U., Hof mann, H. - J . , Sewe, K. -U. and Lindoerfer, W. (1985)
Process for t he biotechnological product i on of rhamnol i pi ds and rhamnol i pi ds with only one 13-
hydroxydecanecarboxylic acid moiety in t he molecule. European Pat ent Appl. EP 0156373, Pub.
2 Oct 1985. Appl . US 594223, filed 28 Mar 1984.
665 Tanaka, A. and Fukui , S. (1985) Bioconversion of lipophilic compounds by immobilized biocata-
lysts in t he presence of organic solvents. Biotechnol. Ser. 5, 149- 176.
666 Caunt , P. (1987) Immobi l i zat i on of cells in a linear polyacrylamide matrix: Degradat i on of a mix-
t ure of volatile fat t y acids by Alcaligenes denitrificans. Biotechnol. Lett. 9, 4 7 - 4 8 .
667 Estival, F. and Burstein, C. (1985) Immobilized thermophilic bact eri a as a source of respiratory
chai n for t he recycling of NAD. Enzyme Mi crob. Technol. 7, 2 9 - 3 3 .
668 Mat sunaga, T., Mat sunaga, N. and Ni shi mura, S. (1985) Regeneration of NAD(P)H by immobili-
zed whole cells of Clostridium but yri cum under hydrogen high pressure. Biotechnol. Bioeng. 27(9),
1277- 1281.
669 Sakai, T., Nakamur a, T., Fukuda, K. and Amano, E. (1986) Highly enantoselective reduction of
ethyl-2-acyloxy-3-oxobutanoate with immobilized baker s' yeast. Bull. Chem. Soc. Jpn. , 59,
3185- 3188.
670 Sonleitner, B. and Fiechter, A. (1986) Application of immobilized cells of Thermoanaerobium brockii
for stereoselective reductions of oxo-acid esters. Appl. Microbiol. Biotechnol. 23(6), 424- 429.
671 Hi l debrand, H. , Zi t zmann, W., Arl t , D. and Koelbl, H. (1985) Process for the product i on of cyclo-
propane carboxylic acids. European Pat ent Appl. EP 0164573, Pub. 18 Dec 1985, Appl. DE 3418374,
filed 17 May 1984.
672 Bailliez, C., Largeau, C. and Casadevall, E. (1985) Growt h and hydrocarbon product i on of Bot ry-
ococcus braunii immobilized in calcium alginate gel. Appl. Microbiol. Biotechnol. 23(2), 9 9 - 105.
673 Robins, R. J. and Rhodes, M. J. C. (1986) The st i mul at i on of ant hr aqui none product i on by Cincho-
na ledgeriana cultures with polymeric adsorbent s. Appl . Microbiol. Biotechnol. 24(1), 3 5 - 41.
674 Nicolaus, B., de Simone, A. , del Pi ano, L., Gi ardi na, P. and Lama, L. (1986) Pr oduct i on of
2-keto-3-deoxygluconate by immobilized cells of Sul f ol obus solfataricus. Biotechnol. Lett. 8(7),
497 - 500.
675 Thepenier, C., Gudi n, C. and Thomas, D. (1985) Immobi l i zat i on of Porphyri di um cruentum in
pol yuret hane foams for t he product i on of polysaccharide. Biomass, 7, 225- 240.
676 Evans, P. J . and Wang, H. Y. (1984) Pi gment product i on from immobilized Monascus species utili-
zing polymeric resin adsorpt i on. Appl . Envi ron. Microbiol. 47, 1323- 1326.
677 Kahl on, S.S. and Mal hot ra, S. (1986) Pr oduct i on of gibberellic acid by fungal mycelium immobili-
zed in sodium alginate. Enzyme Microb. Technol. 8(10), 613- 616.
678 Anon. (1986) Mass product i on of gl ut at hi one using bioreactor. Biotechnol. Jpn. Newsserv. 4(12), 5.
679 Tosa, T. (1983) Pr oduct i on of water-soluble compounds in bi oreact ors and its industrial applicati-
on. Saibo Kogaku, 2, 3 5 3 - 359.
680 Yongsmith, B. and Chut i ma, K. (1983) Pr oduct i on of vi t ami n B12 by living bacterial cells i mmobi -
lized in calcium alginate gels. J. Ferment . Technol. 61, 593- 598.
90
681 Roland, J. F. , Cayle, T., Dinwoodie, R.C. and Mehnert, D.W. (1985) Bioconversion production
of ascorbic acid. PCT Patent Appl. WO 85/01745. Publ. 25 Apr 1985. Appl. US 543975, filed 20
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682 Baklashova, T.G., Koscheenko, K.A. and Skryabin, G.K. (1984) Hydroxylation of indolyl-3-acetic
acid by immobilized mycelium of Aspergillus niger. Appl. Microbiol. Biotechnol. 19, 217- 223.
683 Kole, M. M. and Altosaar, I. (1985) Conversion of chenodeoxycholic acid to ursodeoxycholic acid
by Clostridium absonum in culture and by immobilized cells. Microbiol. Lett. 28(1), 69- 72.
684 Uzura, K., Owaki, J., Minami, Z. and Kusai, K. (1986) Enzymic conversion of dihydrouracil into
uracil. J. Ferment. Technol. 64(3), 199-203.
685 Brookes, I.K., Lilly, M. D. and Drozd, J. W. (1987) Use of immobilized Bacillus subtilis for the
stereospecific hydrolysis of D,L-menthyl acetate. Enzyme Microb. Technol. 9, 217-220.
686 Shirai, K. (1987) Cathecol production from benzene through reaction with resting and immobilized
cells of a mutant strain of Pseudornonas. Agric. Biol. Chem. 51, 121 - 128.
687 Caunt, P. and Chase, H. A. (1987) Degradation of n-valeric acid by alginate-entrapped Alcaligenes
denitrificans. Appl. Microbiol. Biotechnol. 25, 453-458.
688 Sato, N., Murata, K. and Kimura, A. (1986) Depolymerization of chondroitin C sulphate by immo-
bilized Proteus vulgaris cells. Biotechnol. Bioeng. 28, 1707- 1712.
689 Davidenko, T. I., Kotlyar, 1. I., Bondarenko, G.I. and Kabanov, V.M. (1984) Reduction of nitro
derivatives of 1,2-dihydro-3H- 1,4-benzodiazepin-2-ones by immobilized Escherichia coil cells. Khim.
Farm. Zh. 18, 1105-1110.
690 Huang, T.-L., Fang, B.-S. and Fang, H.-Y. (1985) Oxidation of secondary alcohols to methyl ke-
tones by immobilized yeast cells. J. Gen. Appl. Microbiol. 31(2), 125 - 134.
691 Mironowicz, A. and Siewinski, A. (1986) Biotransformations. X1X. Reduction of some terpenic
ketones by means of immobilized cells of Rhodotorula mucilaginosa. Acta Biotechnol. 6(2), 141 - 146.
692 Cambiaghi, S., Dallatomasina, F., Giardino, P., Murador, E. and Spreafico, G. (1986) Process
for preparing peptides. UK Patent Appl. GB 2160870. Pub. 2 Jan 1986. Appl. IT 21622, filed 27
Jun 1984.