J OU RN AL OF STRU CTU RAL BIOLOGY

ARTICLE N O. SB984062

124, 311334 (1998)

Cyanobacterial Phycobilisomes
Rober t Ma cColl
Wad sw orth Cen ter, N ew York S tate Departm en t of H ealth , P.O. B ox 509, Alban y, N ew York 12201-0509
Received J u ly 9, 1998, a n d in r evised for m Novem ber 11, 1998

a lly t o ph ot osyst em II. Wh en t h e en er gy a bsor bed by

t h e ch r om opr ot ein s (bilipr ot ein s) of t h e ph ycobilisom es r ea ch es t h e r ea ct ion cen t er s of ph ot osyst em
II, t h er e occu r s a t r a n sdu ct ion of t h e excit a t ion
en er gy t o ch em ica l en er gy. Bilipr ot ein s a bsor b r a dia t ion in r egion s of t h e visible spect r u m wh er e ch lor oph yll a h a s low a bsor pt ivit ies. P h ycobilisom es a r e
pr esen t in pr oca r yot ic cya n oba ct er ia a n d eu ca r yot ic
r ed a lga e. Alt h ou gh t h is r eview fea t u r es cya n oba ct er ia l ph ycobilisom es, wh en per t in en t , r ed a lga l ph ycobilisom es a n d bilipr ot ein s will be m en t ion ed select ively. Th e com posit ion of ph ycobilisom es va r ies fr om
or ga n ism t o or ga n ism , a n d in dividu a l or ga n ism s
h a ve ph ycobilisom es t h a t a r e ch a n ged by t h e en vir on m en t in diver se wa ys.
Th e begin n in g of st u dy of t h e ph ycobilisom e ca m e
in 19651966 wh en Ga n t t a n d Con t i, u sin g r ed
a lga e, per for m ed a ser ies of exper im en t s t h a t r esu lt ed in t h e isola t ion of ext r in sic gr a n u les fr om t h e
ou t er or st r om a l su r fa ce of t h e ch lor oph yll acon t a in in g t h yla koid m em br a n e. Th ese wa t er-solu ble
isola t es wer e sh own t o con t a in t h e bilipr ot ein s of t h e
a lga e (Ga n t t a n d Con t i, 1965, 1966a , 1966b).
F ollowin g t h is lea d, ot h er r esea r ch sh owed by
elect r on m icr oscopy t h a t cya n oba ct er ia a n d cya n elles likewise con t a in ph ycobilisom es (Wildm a n
a n d Bowen , 1974; E dwa r ds a n d Ga n t t , 1971; Ga n t t
a n d Con t i, 1969; Bou r du a n d Lefor t , 1967; Lefor t ,
1965; E dwa r ds et al., 1968). Th er e a r e differ en t
st r u ct u r a l t ypes of ph ycobilisom es, bu t in t h is r eview
t h e h em idiscoida l ph ycobilisom es h a vin g a t r icylin dr ica l cor e a n d six r ods, wh ich a r e fou n d ext en sively
in t h e cya n oba ct er ia , will be discu ssed in m ost det a il.
Th e h em idiscoida l ph ycobilisom es a r e divided in t o
t h r ee cor e t ypes: bicylin dr ica l; t r icylin dr ica l (F ig. 1);
a n d pen t a cylin dr ica l (Du cr et et al., 1996, 1998; Sidler,
1994; Ya m a n a ka et al., 1980; Willia m s et al., 1980;
Gla u ser et al., 1992a ; Ison o a n d Ka t oh , 1983, 1987).
Th e pen t a cylin dr ica l ph ycobilisom es h a ve eigh t r ods
a ssocia t ed wit h a five-cylin der cor e. In a ddit ion t o
t h e h em idiscoida l t ypes, t h er e a r e ot h er st r u ct u r a lly
differ en t ph ycobilisom es: h em iellipsoida l, bu n dlesh a ped, block-sh a ped, a n d h em iellidiscoida l (Du cr et
et al., 1998; Weh r m eyer et al., 1988; Weh r m eyer,

Cy a n o ba c te ria l p h y c o bilis o m e s h a rv e s t lig h t a n d

c a u s e e n e rg y m ig ra tio n u s u a lly to w a rd p h o to s y s te m II re a c tio n c e n te rs . En e rg y tra n s fe r fro m p h y c o bilis o m e s d ire c tly to p h o to s y s te m I m a y o c c u r u n d e r
c e rta in lig h t c o n d itio n s . Th e p h y c o bilis o m e s a re
h ig h ly o rg a n ize d c o m p le x e s o f v a rio u s bilip ro te in s
a n d lin k e r p o ly p e p tid e s . P h y c o bilis o m e s a re c o m p o s e d o f ro d s a n d a c o re . Th e bilip ro te in s h a v e th e ir
bilin s (c h ro m o p h o re s ) a rra n g e d to p ro d u c e ra p id
a n d d ire c tio n a l e n e rg y m ig ra tio n th ro u g h th e p h y c o bilis o m e s a n d to c h lo ro p h y ll a in th e th y la k o id
m e m bra n e . Th e m o d u la tio n o f th e e n e rg y le v e ls o f
th e fo u r c h e m ic a lly d iffe re n t bilin s by a v a rie ty o f
in fl u e n c e s p ro d u c e s m o re e ffic ie n t lig h t h a rv e s tin g
a n d e n e rg y m ig ra tio n . Ac c lim a tio n o f c y a n o ba c te ria l p h y c o bilis o m e s to g ro w th lig h t by c o m p le m e n ta ry c h ro m a tic a d a p ta tio n is a c o m p le x p ro c e s s th a t
c h a n g e s th e ra tio o f p h y c o c y a n in to p h y c o e ry th rin
in ro d s o f c e rta in p h y c o bilis o m e s to im p ro v e lig h t
h a rv e s tin g in c h a n g in g h a bita ts . Th e lin k e rs g o v e rn
th e a s s e m bly o f th e bilip ro te in s in to p h y c o bilis o m e s , a n d , e v e n if c o lo rle s s , in c e rta in c a s e s th e y
h a v e be e n s h o w n to im p ro v e th e e n e rg y m ig ra tio n
p ro c e s s . Th e L c m p o ly p e p tid e h a s s e v e ra l fu n c tio n s ,
in c lu d in g th e lin k e r fu n c tio n o f d e te rm in in g th e
o rg a n iza tio n o f th e p h y c o bilis o m e c o re s . D e ta ils o f
h o w lin k e rs p e rfo rm th e ir ta s k s a re s till to p ic s o f
in te re s t. Th e tra n s fe r o f e x c ita tio n e n e rg y fro m bilin
to bilin is c o n s id e re d , p a rtic u la rly fo r m o n o m e rs
a n d trim e rs o f C-p h y c o c y a n in , p h y c o e ry th ro c y a n in ,
a n d a llo p h y c o c y a n in . P h y c o bilis o m e s a re o n e o f th e
w a y s c y a n o ba c te ria th riv e in v a ry in g a n d s o m e tim e s e x tre m e h a bita ts . Va rio u s bilip ro te in p ro p e rtie s p e rh a p s n o t re la te d to p h o to s y n th e s is a re c o n s id e re d : th e p h o to re v e rs ibility o f p h y c o v io lo bilin ,
b i o p h y s i c a l s t u d i e s , a n d b i li p ro t e i n s i n e v o lu tio n . r 1998 Ac a d e m ic P re s s
K ey Wor d s : b i li p ro t e i n s ; c o m p le m e n t a ry c h ro m a tic a d a p ta tio n ; e n e rg y m ig ra tio n in p h o to s y n th e s is ; p h y c o bilis o m e s .
P HYCOB ILIS OMES

P h ycobilisom es a r e pr ot ein com plexes t h a t fu n ct ion in ligh t h a r vest in g a n d en er gy m igr a t ion , u su 311

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ROBE RT MACCOLL

1983). A cya n oba ct er iu m wit h bilipr ot ein s n ot or ga n ized in t o ph ycobilisom es h a s a lso been r epor t ed
(Reu t er et al., 1994).
Th e wor k of Ga n t t a n d co-wor ker s (e.g., Ga n t t a n d
Con t i, 1965, 1966a , 1966b; Ga n t t a n d Lipsch u lt z,
1973, 1977; Ga n t t et al., 1976, 1988; Mim u r o et al.,
1986b; Redlin ger a n d Ga n t t , 1981, 1982) wa s sem in a l. In t h e m or e t h a n t h r ee deca des sin ce t h e or igin a l br ea kt h r ou gh , t h er e h a s been excit in g pr ogr ess.
Th e t ech n iqu es of bioch em ist r y, m olecu la r biology,
spect r oscopy, x-r a y diffr a ct ion , elect r on m icr oscopy,
a n d bioph ysics h a ve ser ved t o a dd t o t h e u n der st a n din g of t h e wa y t h ese gr a n u les per for m t h eir fu n ct ion s
in ph ot osyn t h esis. Th er e a r e pr eviou s r eviews on
cer t a in of t h ese t opics (e.g., Sidler, 1994; Ga n t t ,
1975, 1990; Sch eer, 1987; Ma cColl a n d Gu a r d-F r ia r,
1987; Th om a s, 1989; Zu ber, 1987; Br ya n t , 1991;
St a dn ich u k, 1995).
Bilipr ot ein s a r e ca t egor ized in t o t h r ee t ypes by
bilin en er gy: t h ose of h igh en er gy (ph ycoer yt h r in s or
ph ycoer yt h r ocya n in ), in t er m edia t e en er gy (ph ycocya n in s), a n d low en er gy (a lloph ycocya n in s). E n er gy
will flow fr om h igh est - t o lowest -en er gy pigm en t s
a n d t h is is h ow t h e ph ycobilisom es a r e or ga n ized
(F ig. 1). Th er e a r e six r ods in h em idiscoida l ph ycobilisom es h a vin g t h r ee cylin der s in t h eir cor e. Th e cor e
is sit u a t ed in pr oxim it y t o t h e t h yla koid m em br a n e
a n d ph ot osyst em II, wh er e ch lor oph yll a is loca t ed
(F igs. 1 a n d 2). Th e r ods h a ve t h e ph ycoer yt h r in or
ph ycoer yt h r ocya n in , if eit h er is pr esen t , fu r t h est
fr om t h e cor e. Th e cor e h a s t h e a lloph ycocya n in s, of
wh ich t h er e a r e t wo fu n ct ion a l t ypes: a lloph ycocya n in h a vin g a 650-n m m a xim u m a n d t wo loweren er gy a lloph ycocya n in s, t h e L cm polypept ide a n d

F IG. 1. Model of a t r icylin dr ica l h em idiscoida l ph ycobilisom e.

In t h e u pper dr a win g, t h e ph ycobilisom e is sh own a t t a ch ed t o
ph ot osyst em II. Two ph ot osyst em I pa r t icles a r e sh own a dja cen t
t o t h e ph ot osyst em II pa r t icle. A t r icylin dr ica l cor e is sh own , a n d
t h e t wo bot t om cylin der s a t t a ch t o t h e t h yla koid m em br a n e. Th e
t wo ba sa l cylin der s t h a t a r e a t t a ch ed t o t h e m em br a n e will ea ch
be ca lled A, a n d t h e cylin der loca t ed a bove t h em will be ca lled B or
t op cylin der.

F IG. 2. P h ycobilisom e det a ils. Th e cor e con t a in s t h e a lloph ycocya n in s a n d a t t a ch es t o t h e t h yla koid m em br a n e. Th e bot t om
t wo cylin der s, t h e ba sa l or A cylin der s, a r e a t t a ch ed t o t h e
t h yla koid m em br a n e. Th e r od con t a in s ph ycocya n in a n d, wh en
pr esen t , ph ycoer yt h r in or ph ycoer yt h r ocya n in . Th e cor e com plexes a r e t r im er or t r im er-like com plexes: (1) a3 b3 L 8.9
c ; (2) a3 b3 ;
(3) a2 b2 b16 L cm ; a n d (4) aB a2 b3 L 8.9
c . Wh er e a a n d b a r e t h e su bu n it s
8.9
of a lloph ycocya n in , L c is a cor e lin ker, b16 is a bilin -con t a in in g
polypept ide, a n d L cm a n d aB a r e t h e t wo lower-en er gy a lloph ycocya n in s. Th e t wo cylin der s a dja cen t t o t h e t h yla koid m em br a n e a r e
com posed of on e copy ea ch of com plexes 14. Th e t h ir d cylin der,
t h e B or t op cylin der, is com posed of t wo copies ea ch of com plexes 1
a n d 2. Th e side view of t h e cor e sh ows t wo of t h e cylin der s a n d t h e
t h ir d is h idden . Sin ce t h er e a r e fou r t r im er s per cylin der, t h e t ot a l
n u m ber of t r im er s is 12 in it s cor e.

t h e aB polypept ide, wh ich t r a n sfer en er gy t o ch lor oph yll (Ga n t t , 1975; Ma cColl a n d Gu a r d-F r ia r, 1987;
Br ya n t et al., 1979; Sidler, 1994; Ba ld et al., 1996).
Th e r ods a r e com posed of st a cks of disks, a n d t h e
disk a dja cen t t o t h e cor e is in va r ia bly ph ycocya n in .
Dividin g t h e bilin s in t o r ods will m a ke it sim pler t o
h a ve a r r a n gem en t s of t h e bilin s for efficien t en er gy
t r a n sfer. Th er e a r e t ypica lly t wo t o six disks in a r od
depen din g on t h e or ga n ism a n d t h e im pa ct of t h e
en vir on m en t .
Ta n dea u de Ma r sa c a n d Coh en -Ba zir e (1977) pr opelled t h e u n der st a n din g of ph ycobilisom es t o a
h igh er level wit h t h e discover y of t h e lin ker polypept ides. Th eir wor k wa s a ll t h e m or e ou t st a n din g
beca u se, pr ior t o t h eir 1977 pu blica t ion , t h er e wa s n o
h in t of t h ese lin ker s. Th ey fou n d t h a t a n ew gr ou p of
polypept ides exist ed wit h in t h e ph ycobilisom es, a n d
it is n ow kn own t h a t m ost of t h ese a r e color less wh ile
ot h er s h a ve ch r om oph or es, like t h e bilipr ot ein s. Ta n dea u de Ma r sa c a n d Coh en -Ba zir e (1977) poin t ed
ou t t h a t t h e lin ker s wou ld fu n ct ion in a t t a ch in g t h e

P H YCOBILISOME S

ph ycobilisom es t o t h e t h yla koid m em br a n e a n d in

a ssem bly of t h e bilipr ot ein s. E xper im en t s u sin g pu r ified lin ker s a n d bilipr ot ein pr ovided dir ect eviden ce
t h a t lin ker s fu n ct ion in a ssem bly of bilipr ot ein s
(Lu n dell et al., 1981a ). As cer t a in of t h e lin ker s ca u se
a ssem bly of t h e bilipr ot ein s, t h ey pr odu ce ch a n ges in
t h e spect r a of bilipr ot ein s, a n d t h is m a y ser ve t o
dir ect en er gy m igr a t ion m or e efficien t ly t h r ou gh t h e
ph ycobilisom es (Yu et al., 1981; Wen dler et al., 1986).
Lin ker s a r e fou n d in bot h cya n oba ct er ia l a n d r ed
a lga e ph ycobilisom es a n d m a y be 1015% of t h e t ot a l
m a ss (Ta n dea u de Ma r sa c a n d Coh en -Ba zir e, 1977;
Ya m a n a ka et al., 1978; Koller et al., 1978).
B ILIP ROTEIN S

Bilipr ot ein s of t h e cya n oba ct er ia a r e obt a in ed a s

dissocia t ion pr odu ct s of t h e ph ycobilisom es. Wh en
t h e pr oca r yot ic cells a r e br oken a n d t h e cellu la r
con t en t s esca pe in t o a low-ion ic-st r en gt h a qu eou s
m ediu m , t h e ph ycobilisom es dissocia t e in t o t h e va r iou s com pon en t s, a n d t h e bilipr ot ein s, eit h er wit h or
wit h ou t a t t a ch ed lin ker s, a r e obt a in ed for a n a lysis.
Th e r ela t ive st a bilit y of bilipr ot ein lin ker com plexes
va r ies a m on g t h e bilipr ot ein s a n d differ en t sou r ces.
Alloph ycocya n in , wit h a 650-n m m a xim u m , is fou n d
n ea r n eu t r a l pH a s a t r im er h a vin g t h r ee a a n d t h r ee
b polypept ides; ea ch of t h ese polypept ides h a s on e
ch r om oph or e (bilin ). Tr im er s (a3 b3 ) a r e r in glike a ssem blies of t h r ee m on om er s (ab) h a vin g t h r eefold
sym m et r y. C-P h ycocya n in is fou n d a s a com plex
solu t ion of a3 b3 , a6 b6 , a n d ot h er oligom er s. Th e
h exa m er s (a6 b6 ) a r e disk sh a ped, for m ed by fa ce-t ofa ce a ssem bly of t r im er s. Rods a r e for m ed by fa ce-t ofa ce a ssem bly of t h ese disks. Th e a polypept ide h a s
on e ch r om oph or e a n d b h a s t wo. C-P h ycoer yt h r in ,
wh ich a lso a ssem bles t o disks, h a s a n a polypept ide
wit h t wo ch r om oph or es a n d a b wit h t h r ee. Th ese a
a n d b polypept ides va r y in m olecu la r m a ss fr om
15 000 t o 20 000 Da .
Mon om er s (ab) of a lloph ycocya n in a n d C-ph ycocya n in a r e of in t er est in t h e st u dy of bilipr ot ein s beca u se t h ey r epr esen t m in im u m u n it s h a vin g a ll t h e
bilin s. H om ogen eou s a n d st a ble m on om er s of t h ese
bilipr ot ein s ca n be pr epa r ed a t a sligh t ly a cid pH or
in t h e pr esen ce of t h e ch a ot r opic a n ion s t h iocya n a t e
or per ch lor a t e (Ma cColl, 1983; Ma cColl et al., 1971,
1980, 1981). Th e ch a ot r opes a r e m or e u n iver sa lly
a pplica ble. F or a t h er m oph ilic pr ot ein , a h igh er
ch a ot r ope con cen t r a t ion is n eeded t o pr odu ce m on om er s (E dwa r ds et al., 1997). Mon om er s of ph ycoer yt h r ocya n in h a ve been pr epa r ed u sin g u r ea or ch a ot r ope (Siebzen r u bl et al., 1989). Mon om er s ca n be
pr odu ced, wit h ou t a dissocia t in g a gen t n ea r n eu t r a l
pH , a t a ver y low pr ot ein con cen t r a t ion (Ma cColl a n d
Gu a r d-F r ia r, 1987). Bilipr ot ein s ca n be com plet ely
dissocia t ed in t o t h e in dividu a l a a n d b polypept ides

313

by va r iou s den a t u r in g a gen t s (Ma cColl a n d Gu a r dF r ia r, 1987).

Th e det er m in a t ion of t h e a m in o a cid sequ en ces of
va r iou s bilipr ot ein s h a s been a n im por t a n t st ep in
u n der st a n din g t h eir pr oper t ies. Zu ber a n d cowor ker s obt a in ed t h e fir st com plet e a m in o a cid sequ en ces of a n y bilipr ot ein u sin g cya n oba ct er ia l Cph ycocya n in a n d a lloph ycocya n in (F r a n k et al., 1978;
Sidler et al., 1981), a n d Tr oxler a n d co-wor ker s did
likewise for r ed a lga l C-ph ycocya n in a n d a lloph ycocya n in (Offn er et al., 1981; Tr oxler et al., 1981; Offn er
a n d Tr oxler, 1983). Th er e is sign ifica n t h om ology
a m on g t h e va r iou s bilipr ot ein s. Th er e is ver y ou t st a n din g con ser va t ion of t h e pla cem en t of t h e bilin s
in t h e a m in o a cid sequ en ce.
Th e com plet e sequ en ce of t h e a m in o a cids is a lso
kn own for ph ycoer yt h r ocya n in (F u glist a ller et al.,
1983). Th e bilin s a r e loca t ed a t a84, b84, a n d b155.
Th er e is a 21% h om ology bet ween t h e t wo polypept ides, 63% h om ology of a a n d 67% h om ology of b t o
t h e a a n d b polypept ides of C-ph ycocya n in , r espect ively. Sidler et al. (1986) h a ve obt a in ed t h e a m in o
a cid sequ en ce for C-ph ycoer yt h r in . F or t h is cya n oba ct er ia l bilipr ot ein t h er e a r e five bilin s, t wo on t h e a
polypept ide a n d t h r ee on b. Th e bilin s a r e bou n d t o
cyst ein es a t a84 a n d a143, a n d t h er e is a bilin dou bly
bou n d t o b50 a n d b61. Th e r em a in in g t wo bilin s a r e
a t t a ch ed a t b84 a n d b155. A CU-ph ycoer yt h r in h a s
a lso been sequ en ced (Wilba n ks et al., 1991).
Th e bilin s a r e open -ch a in t et r a pyr r oles (F ig. 3),
wh ich a r e cova len t ly a t t a ch ed t o a popr ot ein by
t h ioet h er bon ds t o pa r t icu la r cyst ein e r esidu es
(F ig. 4). In t h e m a n y cya n oba ct er ia , t h er e a ppea r t o
be fou r differ en t bilin s (Ta ble I): ph ycocya n obilin ,
ph ycoer yt h r obilin , ph ycou r obilin , a n d ph ycoviolobilin (a lso ca lled ph ycobiliviolin ). Th ey a r e a t t a ch ed
t h r ou gh t h eir A r in gs or h a ve join t a t t a ch m en t s t o
t h eir A a n d D r in gs (F ig. 3) (Ma cColl a n d Gu a r dF r ia r, 1987; Bish op et al., 1987). C-P h ycocya n in a n d
a lloph ycocya n in h a ve ph ycocya n obilin s a n d C-ph ycoer yt h r in h a s ph ycoer yt h r obilin s (Ta ble II). Met a l
ion s a r e n ot a ssocia t ed wit h t h e bilin s.
Besides C-ph ycocya n in , a lloph ycocya n in , a n d Cph ycoer yt h r in , cer t a in cya n oba ct er ia possess du a lbilin bilipr ot ein s, in clu din g t h e CU-ph ycoer yt h r in s,
ph ycoer yt h r ocya n in , R-ph ycocya n in II, a n d a u n iqu e
ph ycocya n in pr ocessin g on e u r obilin a n d t wo ph ycocya n obilin s (ca lled ph ycocya n in WH 8501) (H offm a n
et al., 1990; Swa n son et al., 1991; St a dn ich u k, 1993;
On g a n d Gla zer, 1987; F u jit a a n d Sch im u r a , 1974;
Rippka et al., 1974; Br ya n t et al., 1981; Ku r sa r et al.,
1981; On g et al., 1984; St a dn ich u k et al., 1985; Cox et
al., 1985; La r ku m et al., 1987; P a r r y, 1988; On g a n d
Gla zer, 1991; H ir ose et al., 1969; Br ya n t et al., 1976).
Th e CU-ph ycoer yt h r in s con t a in ph ycou r obilin in a ddit ion t o ph ycoer yt h r obilin , a com m on bilin com bin a -

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ROBE RT MACCOLL

F IG. 3.

St r u ct u r es of select ed bilin s.

t ion in r ed a lga l ph ycoer yt h r in s. P h ycoer yt h r ocya n in con t a in s ph ycoviolobilin a n d ph ycocya n obilin .

R-P h ycocya n in II h a s bot h ph ycocya n obilin a n d ph ycoer yt h r obilin (Ta ble II), a n d t h e ph ycocya n obilin is
a t b84, a n d t h e ph ycoer yt h r obilin s a r e a t b155 a n d
a84, wh ich a r e t h e sa m e bilin loca t ion s a s Cph ycocya n in a n d ph ycoer yt h r ocya n in (On g a n d
Gla zer, 1987). St a dn ich u k (1995) h a s r eviewed st u dies on bilin con t en t .
Th e CU-ph ycoer yt h r in s, fir st obser ved in cya n oba ct er ia l ext r a ct s by H ir ose et al. (1969), a r e a ver y
diver se gr ou p of bilipr ot ein s. Th e C in dica t es a
cya n oba ct er ia l sou r ce for t h e bilipr ot ein , a n d Cph ycoer yt h r in con t a in s ph ycoer yt h r obilin . A CUph ycoer yt h r in h a s ph ycou r obilin in a ddit ion t o ph ycoer yt h r obilin . Th eir m u lt ifa cet ed diver sit y defin es
t h em a s a gr ou p. Th e fir st a spect of t h is diver sit y is
t h a t t h e r a t io of t h e t wo bilin s va r ies widely fr om
pr ot ein t o pr ot ein (On g a n d Gla zer, 1991). F or exa m ple, on e pa r t icu la r CU-ph ycoer yt h r in h a s fou r
ph ycou r obilin s a n d on e ph ycoer yt h r obilin on a m on om er a n d a n ot h er h a s fou r ph ycoer yt h r obilin s a n d
t wo ph ycou r obilin s (Ta ble III). Th e n u m ber of bilin s
per m on om er differ s, bein g eit h er 5 or 6. Th ose wit h
five bilin s h a ve t h r ee on t h e b polypept ide a n d t wo on
a, a n d t h ose wit h six h a ve a n a ddit ion a l ph ycou r obi-

F IG. 4. P osit ion in g of bilin s in t h e a m in o a cid sequ en ces of

cer t a in bilipr ot ein s: C-ph ycoer yt h r in , C-ph ycocya n in , a n d a lloph ycocya n in . P E B a n d P CB a r e ph ycoer yt h r obilin a n d ph ycocya n obilin , r espect ively.

lin on a. Th er e m a y be t wo differ en t ph ycoer yt h r in s

per cya n oba ct er iu m . In som e ca ses, a CU-ph ycoer yt h r in m a y be fou n d wit h a C-ph ycoer yt h r in (On g a n d
Gla zer, 1991; St a dn ich u k, 1993), a n d in ot h er cya n oba ct er ia t h er e m a y be t wo differ en t CU-ph ycoer yt h r in s. A pr epa r a t ion of CU-ph ycoer yt h r in h a d t h e
m olecu la r m a ss of a t ypica l disk, a6 b6 g, of a ph ycobilisom e r od (On g et al., 1984). Wh en t h e polypept ides
wer e sepa r a t ed, in a ddit ion t o a a n d b, t h er e wer e
TAB LE I
Bilin s of Cya n oba ct er ia l Bilipr ot ein s
Bilin a

Con ju ga t ed dou ble bon ds b

P h ycocya n obilin
P h ycoer yt h r obilin
P h ycoviolobilin
P h ycou r obilin

8
6
7
5

Bish op et al. (1987) for st r u ct u r es.

Mor e con ju ga t ion for a bilin pr odu ces lower en er gy for t h e fir st
excit ed st a t e. F or exa m ple, C-ph ycocya n in m on om er s h a ve on ly
ph ycocya n obilin s a n d u su a lly h a ve a 614-n m a bsor pt ion m a xim u m . Th e ph ycou r obilin s in CU-ph ycoer yt h r in h a ve a n a bsor pt ion m a xim u m a t 495 n m .
b

315

P H YCOBILISOME S

t h r ee r ed ba n ds of a r ou n d 29 000 m olecu la r m a ss
t h e expect ed va lu e of r od-r ela t ed lin ker s. Wh en
lin ker s fr om t h e r ods bea r bilin s, t h ey a r e n a m ed g
polypept ides. Lin ker s fr om r ods of C-ph ycocya n in
a n d C-ph ycoer yt h r in a r e pr oba bly color less. On e
lin ker fr om a CU-ph ycoer yt h r in h a s been sequ en ced
a n d sh own t o h a ve a sin gle ph ycou r obilin (Wilba n ks
a n d Gla zer, 1993). Su ch bilin diver sifica t ion sign ifies
ligh t h a r vest in g a s a n im por t a n t a spect of t h e ecology for t h ese or ga n ism s.
Bilipr ot ein s fu n ct ion in ph ot osyn t h esis by h a r vest in g sola r en er gy in r egion s wh er e ch lor oph yll a
a bsor bs poor ly, ca u sin g t h is en er gy t o m igr a t e wit h
gr ea t efficien cy fr om t h e poin t of a bsor pt ion t owa r d a
r ea ct ion cen t er. It is im por t a n t t h a t bilipr ot ein s
a bsor b ph ot on s over wide r a n ges of en er gies. Th e
va r iou s bilin s a ch ieve a diver sit y of ligh t a bsor pt ion
in it ia lly beca u se of t h e va r ia t ion s in t h eir syst em s of
con ju ga t ed dou ble bon ds (F ig. 3). P h ycocya n obilin
h a s m or e con ju ga t ion t h a n ph ycoer yt h r obilin so solu t ion s of ph ycocya n in n ea r n eu t r a l pH a bsor b a t lower
en er gy (610- t o 620-n m m a xim u m ) t h a n ph ycoer yt h r in (545- t o 565-n m m a xim u m ). P h ycou r obilin h a s
st ill less con ju ga t ion (st r u ct u r e n ot sh own ) a n d
a bsor bs m a xim a lly a r ou n d 495 n m , a h igh er en er gy

TAB LE II
Cya n oba ct er ia l Bilipr ot ein s

Bilipr ot ein
C-P h ycocya n in
C-P h ycoer yt h r in
Alloph ycocya n in s
CU-P h ycoer yt h r in s
P h ycoer yt h r ocya n in
R-P h ycocya n in II
P h ycocya n in WH 8501

Bilin
P h ycocya n obilin
P h ycoer yt h r obilin
P h ycocya n obilin s
P h ycoer yt h r obilin ,
ph ycou r obilin
P h ycocya n obilin , ph ycoviolobilin
P h ycocya n obilin , ph ycoer yt h r obilin
P h ycocya n obilin , ph ycou r obilin

Su ggest ed
bilipr ot ein
r en a m in g a

CV-ph ycocya n in
CE -ph ycocya n in
CU-ph ycocya n in

a Sin ce t h e pr efix R or igin a lly in dica t ed a r ed a lga l bilipr ot ein ,

t h e n a m e R-ph ycocya n in II is a m bigu ou s. It wou ld be in t er est in g
t o con sider r en a m in g cer t a in cya n oba ct er ia l bilipr ot ein s t o r eflect
t h eir bilin con t en t s. R-ph ycocya n in II m igh t bet t er be design a t ed
CE -ph ycocya n in , in dica t in g t h e ph ycoer yt h r obilin , a n d likewise
ph ycoer yt h r ocya n in wou ld be CV-ph ycocya n in . It ca n be n ot ed
t h a t C-ph ycocya n in , CE -ph ycocya n in , a n d CV-ph ycocya n in a ll
h a ve t h r ee bilin s loca t ed a t a84, b84, a n d b155. Th e cya n oba ct er ia l ph ycocya n in WH 8501 isola t ed by Swa n son et al. (1991),
h a vin g u r obilin a n d ph ycocya n obilin , wou ld fit t h is n om en cla t u r e
n icely a s CU-ph ycocya n in , wh er e t h e C in dica t es a cya n oba ct er ia l
sou r ce a n d t h e U a ph ycou r obilin in a ddit ion t o t h e ph ycocya n obilin . Th e CU-ph ycoer yt h r in s a lr ea dy u se t h is pr ot ocol. Bilin n a m es,
like ph ycocya n obilin , a r e t h e sa m e for fr ee a n d pr ot ein -bou n d
bilin even t h ou gh t h e bin din g t o pr ot ein elim in a t es on e dou ble
bon d. Th e pr efix B in dica t es a cer t a in t ype of r ed a lga , t h e
Ba n gioph yea n s.

TAB LE III
Bilin Loca t ion s a n d Con t en t s for Sever a l
Cya n oba ct er ia l Bilipr ot ein s
Bilin loca t ion a
Bilipr ot ein

a75

Alloph ycocya n in
C-P h ycocya n in
P h ycoer yt h r ocya n in c
R-P h ycocya n in II c
P h ycocya n in WH 8501 c
C-P h ycoer yt h r in
CU-P h ycoer yt h r in (1)
CU-P h ycoer yt h r in (2)
CU-P h ycoer yt h r in (3) P UB
CU-P h ycoer yt h r in (4) P UB

a84
P CB b
P CB
P VB
PEB
P UB
PEB
P UB
PEB
P UB
PEB

a140 b50/61

b84

b155

PEB
P UB
P UB
P UB
PEB

P CB
P CB
P CB
P CB
P CB
PEB
PEB
PEB
PEB
PEB

P CB
P CB
PEB
P CB
PEB
P UB
PEB
PEB
PEB

PEB
P UB
P UB
P UB
P UB

a On g a n d Gla zer (1987); F r a n k et al. (1978); F u

glist a ller et al.
(1983); Swa n son et al. (1991); Sidler et al. (1981, 1986). Th e bilin
a t b84 wa s det er m in ed t o be t h e lowest -en er gy bilin for t h ese
ph ycocya n in s a n d ph ycoer yt h r in s (On g a n d Gla zer, 1987, 1991).
b P CB, ph ycocya n obilin ; P VB, ph ycoviolobilin ; P E B, ph ycoer yt h r obilin ; P UB, ph ycou r obilin .
c See Ta ble II for su ggest ion s on r en a m in g som e of t h ese
cya n oba ct er ia l bilipr ot ein s.

t h a n ph ycoer yt h r obilin s (Ta ble I). Besides bilipr ot ein s h a vin g a pa r t icu la r bilin for ligh t h a r vest in g, a
bilipr ot ein m a y h a ve t wo differ en t bilin s, wh ich
dr a m a t ica lly in cr ea se t h e r a n ge of ph ot on a bsor pt ion . So fa r, n o sin gle cya n oba ct er ia l bilipr ot ein h a s
been discover ed h a vin g t h e ligh t -h a r vest in g a t t r ibu t e of t h r ee differ en t bilin s, a lt h ou gh t h is occu r s
for cr ypt om on a d bilipr ot ein s (Sidler, 1994; Ma cColl
a n d Gu a r d-F r ia r, 1987).
St a r t in g fr om t h e ch em ica l st r u ct u r e of t h e bilin s,
fin e-t u n in g is a pplied t o t h e bilin s t o a ch ieve im pr oved ligh t h a r vest in g a n d en er gy m igr a t ion . Th e
fa ct or s ch a n gin g t h e a bsor pt ivit ies a n d spect r a of
bilin s ca n be con sider ed in six ca t egor ies. F ir st ,
Sch eer a n d Ku fer (1977) h a ve sh own t h a t t h e a popr ot ein ca u ses t h e bilin s t o be m a in t a in ed in a n ext en ded st a t e, wh ich m a xim ize a bsor pt ion in t h e
visible r egion of t h e spect r u m . Wit h ou t t h e in flu en ce
of t h e a popr ot ein , bilin s wou ld t en d t o be m or e cyclic
a n d h a ve low visible a bsor pt ion .
Th e a n a lysis of t h e cr yst a l st r u ct u r es of Cph ycocya n in s pr ovided det a iled in for m a t ion on t h e
bilin s (Sch ir m er et al., 1985, 1987; Du er r in g et al.,
1991). All t h r ee bilin sa84, b84, a n d b155a r e
fou n d t o be ext en ded a n d h a ve sim ila r geom et r ies.
Th e bilin a t b155 differ s in t h e con figu r a t ion of it s D
r in g. Th e in t er a ct ion wit h a popr ot ein est a blish es t h e
bilin geom et r y.
Secon d, t h e bilin s a r e obser ved t o be sin gly or
dou bly a t t a ch ed by t h ioet h er bon ds t o cyst ein e r esidu es of t h e a popr ot ein (F ig. 3).
Th ir d, ch a n ges occu r t h r ou gh in t er a ct ion s in volvin g t h e bilin s a n d t h eir n ea r su r r ou n din gs, r esu lt in g

316

ROBE RT MACCOLL

in gr ea t m odu la t ion of bilin en er gies. E xa m ples

of t h is va r ia bilit y of en er gy a r e t h e in dividu a l ph ycocya n obilin s of C-ph ycocya n in , C-ph ycocya n in /a lloph ycocya n in , a n d t h e 545- a n d 565-n m for m s of
ph ycoer yt h r obilin . E ven t h ou gh C-ph ycocya n in a n d
a lloph ycocya n in h a ve on ly ph ycocya n obilin s, t h eir
a bsor pt ion spect r a a r e sa lien t ly differ en t . Alloph ycocya n in t r im er s h a ve a 650-n m m a xim u m . Th e a bsor pt ion m a xim u m of C-ph ycocya n in t r im er s is a bou t
620 n m . E ven wit h in C-ph ycocya n in , t h e t h r ee ph ycocya n obilin s on a n ab u n it h a ve ver y differ en t
en er gies (Siebzeh n r u bl et al., 1987; Debr eczen y et
al., 1993; Dem idov a n d Mim u r o, 1995).
F ou r t h , t h e a ggr ega t ion of bilipr ot ein s a ffect s t h e
spect r a of t h e bilipr ot ein s. Mon om er s a n d t r im er s of
a lloph ycocya n in a n d C-ph ycocya n in h a ve ver y differen t a bsor pt ion (Ta ble IV) a n d flu or escen ce spect r a .
F ift h , t h e loca l en vir on m en t of a bilin m a y h a ve a
specia l fa ct or, a n ot h er n ea r by bilin . Two bilin s in
close pr oxim it y a n d pr oper or ien t a t ion m a y u n der go
excit on split t in g. Th e en er gy of t h ese bilin s will be
split in t o h igh - a n d low-en er gy levels, a n d t h is
m odu la t ion of t h e en er gy levels m a y h a ve a pr ofou n d
effect on ligh t h a r vest in g a n d en er gy m igr a t ion .
Alloph ycocya n in t r im er s h a ve been discu ssed a s
possible ca n dida t es for excit on split t in g (Ma cColl et
al., 1980; E din gt on et al., 1995, 1996). Th er e is n o
gen er a l a gr eem en t t h a t excit on split t in g occu r s for
a n y bilipr ot ein .
Sixt h , a n ot h er fa ct or t h a t ca u ses m odifica t ion s of
bilin a bsor pt ion en er gies is t h e lin ker s. Wh en colorless lin ker s isola t ed fr om cya n oba ct er ia in t er a ct
wit h C-ph ycocya n in , t h e en er gies of t h e bilin s ca n be
a ffect ed (Yu et al., 1981; Lu n dell et al., 1981a ;

TAB LE IV
Absor pt ion Ma xim a of P h ycocya n obilin s
in Differ en t Sit u a t ion s
P r ot ein
Alloph ycocya n in
C-P h ycocya n in
C-P h ycocya n in a

Alloph ycocya n in b
C-P h ycocya n in

Con dit ion

Mon om er (ab)
Tr im er (a3 b3 )
ab
a3 b3
a3 b3 1 27-kDa
lin ker
a3 b3 1 32.5-kDa
lin ker
a3 b3 1 8.9-kDa
lin ker (L 8.9
c )
3 bilin s on ab
b155 600 c
a84 624
b84 628

Yu et al. (1981).
F u glist a ller et al. (1987).
c Debr eczen y et al. (1993).
d Dem idov a n d Mim u r o (1995).
e Siebzeh n r u
bl et al. (1987).
b

Absor pt ion m a xim u m (n m )

614
650
614
621
638
629
652
596 d 598600 e
618 616618
625 622624

Got t sch a lk et al., 1991; Sch n eider et al., 1995). Th e

lin ker-fr ee a n d lin ker bilipr ot ein com plexes h a d differ en t opt ica l spect r a a s did differ en t lin ker s plu s
bilipr ot ein (Ta ble IV). A r ed a lga l bilipr ot ein exh ibit s
sim ila r beh a vior (Wa t son et al., 1986). P icosecon d
flu or escen ce kin et ics a lso sh owed differ en ces in t h e
beh a vior of C-ph ycocya n in wit h or wit h ou t lin ker.
Th e bilipr ot ein wit h lin ker h a d fa st er en er gy t r a n sfer (Wen dler et al., 1986). It seem s r ea son a ble t h a t
t h ese n u m er ou s m odifica t ion s of t h e en er gy levels
r esu lt in bet t er ligh t h a r vest in g or im pr oved efficien cy in en er gy m igr a t ion . Bh a ler a o et al. (1991),
h owever, h a ve sh own t h a t r od lin ker polypept ides
m a y h a ve on ly a m in or in flu en ce on en er gy t r a n sfer
in a pa r t icu la r sit u a t ion . Th er e is in for m a t ion t h a t
does su ggest t h a t t h e lin ker n ext t o t h e cor e, L RC , h a s
r ed-sh ift ed t h e spect r u m of it s ph ycocya n in disk t o
opt im ize r od t o cor e en er gy t r a n sfer (Sidler, 1994).
Th er e a r e t wo lower-en er gy for m s of a lloph ycocya n in , aB a n d L cm , bot h of wh ich flu or esce n ea r 680 n m ,
wh ich is sim ila r t o em ission fr om in t a ct ph ycobilisom es a n d is a t lower en er gy t h a n t h e m or e com m on
for m of a lloph ycocya n in . It is u n kn own wh a t com bin a t ion s of t h e a bove fa ct or s ca u se t h e bilin s of aB a n d
L cm t o possess t h is cr it ica lly im por t a n t fea t u r e. It h a s
been r epor t ed t h a t ea ch of t h ese polypept ides h a s
on e ph ycocya n obilin (Gla zer a n d Br ya n t , 1975; Lu n dell et al., 1981b).
In a ddit ion t o t h e st u dies m en t ion ed a lr ea dy,
bilipr ot ein s h a ve been in vest iga t ed by a n u m ber of
per spect ives a n d t ech n iqu es. Bilipr ot ein s h a ve been
exa m in ed in m on ola yer s (Alm og a n d Ber n s, 1983),
m u lt ila yer s (Ya m a za ki et al., 1988), film s (F r a ckowia k et al., 1986; J u szcza k et al., 1991), a n d in
ph ot och em ica l a n d elect r och em ica l st u dies (Ber n s,
1976; H e et al., 1996; E vst ign eev a n d Beka sova ,
1970). Th ey h a ve been st u died in im m u n och em ica l
r esea r ch (Ber n s, 1967), a s flu or escen t la bels in im m u n oa ssa ys (Kr on ick, 1986), a n d a s deu t er a t ed pr ot ein s (Ber n s a n d Ma cColl, 1989). Th e bilipr ot ein s do
n ot n or m a lly con t a in m et a l ion s, bu t m et a l ion ca n be
com plexed t o bilipr ot ein s (P a r k a n d Sa u er, 1991;
Ber n s, 1976; Ch en g et al., 1990; Ma cColl et al., 1994).
Br ya n t (1991) h a s r eviewed t h e ext en sive a n d h igh ly
pr odu ct ive a pplica t ion s of m olecu la r gen et ics t o t h e
st u dy of ph ycobilisom es. H ole bu r n in g t ech n iqu es
h a ve been u sed in t h e st u dy of bilipr ot ein s (Koh ler et
al., 1988a ,b; F eis et al., 1992).
An ext r em ely in t er est in g a spect of bilipr ot ein r esea r ch is t h e obser va t ion of r ever sible ph ot och em ist r y in som e sit u a t ion s. Th er e wer e a n u m ber of ea r ly
key con t r ibu t ion s in t h e st u dy of t h is t ype of ph ot och em ist r y (Bjor n , G. S., 1979; Bjor n , L. O., 1979;
Oh ki a n d F u jit a , 1979; Bjor n a n d Bjor n , 1980; de
Kok et a l., 1981; Mu r a ka m i a n d F u jit a , 1983; Sch eer,
1987). Mor e r ecen t ly, Sch eer a n d co-wor ker s (Sch m idt

P H YCOBILISOME S

et al., 1988; Siebzeh n r u bl et al., 1989; Ma r u t h i Sa i et

al., 1992, 1993; H on g et al., 1993; Sch n eider et al.,
1994, 1996; Zh a o et al., 1995; Zh a o a n d Sch eer, 1995)
h a ve focu sed su ccessfu l effor t s on ph ycoer yt h r ocya n in a n d it s ph ycoviolobilin on t h e a polypept ide.
Siebzen r u bl et al. (1989) h a ve st u died ph ycoer yt h r ocya n in a n d fou n d t h e ph ycoviolobilin t o be t h e
ph ot oa ct ive pa r t of t h e pr ot ein . Th e ph ot oeffect wa s
m a xim a l wh en t h e pr ot ein wa s dissocia t ed t o m on om er s. Con ver sely, t h e ph ot ot r a n sfor m a t ion a lso a ffect ed t h e a ggr ega t ion of pr ot ein . Th e ph ycoviolobilin is obt a in ed wit h a 570-n m a bsor pt ion m a xim u m ;
ir r a dia t ion a t 570 n m ca u ses t h e bilin t o lose a bsorba n ce a t 570 n m a n d sim u lt a n eou sly t o in cr ea se
a bsor ba n ce a t 510 n m . Th e effect cou ld be r ever sed
wit h 510-n m ligh t . F lu or escen ce m ea su r em en t s wer e
per for m ed on t h e t wo spect r a l for m s of t h e bilin
(Ma r u t h i Sa i et al., 1992). Th e 510-n m a bsor bin g
for m h a d lit t le flu or escen ce a n d en er gy t r a n sfer
wou ld occu r efficien t ly on ly fr om t h e 570-n m for m .
Th e isom er iza t ion of ph ycoviolobilin r espon sible for
t h e ph ot och em ist r y h a s been in vest iga t ed (Zh a o a n d
Sch eer, 1995; Zh a o et al., 1995).
In a gr eem en t wit h t h e r esu lt s of Siebzeh n r u bl et
al. (1989), Ku fer a n d Bjor n (1989) isola t ed t h e a
polypept ide of ph ycoer yt h r ocya n in a n d sh owed t h a t
it wa s ph ot or ever sible. Th eor et ica l ca lcu la t ion s h a ve
been per for m ed on t h e r ever sible ph ot och em ist r y of
t h e a polypept ide fr om ph ycoer yt h r ocya n in (Sch a rn a gl a n d F isch er, 1993).
E volu tion an d B iliprotein s
Cya n oba ct er ia a r e pr oca r yot es con t a in in g bilipr ot ein s a n d ch lor oph yll a. Th er e h a ve been r epor t s of
bilipr ot ein s discover ed in pr oca r yot es wit h differ en t
ch lor oph ylls. P h ycocya n in a n d a lloph ycocya n in h a ve
been obser ved in a n or ga n ism con t a in in g ch lor oph yll
d (Ma r qu a r dt et al., 1997). A ph ycoer yt h r in wa s
fou n d in a m a r in e or ga n ism a lso h a vin g ch lor oph yll
a, b, a n d c (H ess et al., 1996). Th is ph ycoer yt h r in
m a y h a ve bot h ph ycou r obilin a n d ph ycoer yt h r obilin
a n d m a y be a n ot h er m em ber of t h e diver se CUph ycoer yt h r in s. Th ese or ga n ism s wer e discu ssed in
t er m s of t h eir im plica t ion s in t h e evolu t ion of ph ot osyn t h et ic life.
P h ycobilisom es a n d t h eir bilipr ot ein s h a ve pr ovided u sefu l clu es con cer n in g t h e evolu t ion of ph ot osyn t h et ic or ga n ism s. Ber n s (1967) m a de t h e fir st
con t r ibu t ion t o t h e r ela t ion sh ips a m on g bilipr ot ein s
fr om t h e pr oca r yot ic a n d eu ca r yot ic ph ycobilisom es.
Usin g a n im m u n och em ica l t ech n iqu e, ph ycocya n in s
fr om cya n oba ct er ia wer e dem on st r a t ed t o be closely
r ela t ed t o ph ycocya n in s fr om r ed a lga e, a n d t h e
sa m e wa s discover ed for t h e r ed a lga l a n d cya n oba ct er ia l ph ycoer yt h r in s. Th is wa s a n im por t a n t ea r ly
m olecu la r dem on st r a t ion t h a t t h e r ed a lga e evolved

317

fr om a cya n oba ct er iu m or a cya n oba ct er iu m -like

ph ot osyn t h et ic or ga n ism . Th er e is eviden ce t h a t
eu ca r yot ic r ed a lga e a r ose fr om en dosym biosis bet ween a pr oca r yot ic cya n oba ct er iu m a n d a n on ph ot osyn t h et ic or ga n ism , wit h t h e cya n oba ct er iu m becom in g t h e ch lor opla st of t h e r esu lt in g r ed a lga . A r ed
a lga t h en u n der wen t a secon d en dosym biot ic even t
t o becom e t h e ch lor opla st of a cr ypt om on a d (e.g.,
P a lm er a n d Delwich e, 1996; McF a dden et al., 1994;
Lu dwig a n d Gibbs, 1985; Gibbs, 1990). Im m u n och em ist r y wa s u sed t o su ggest t h a t t h e bilipr ot ein s of
cya n oba ct er ia , r ed a lga e, a n d t h e cr ypt om on a ds wer e
a ll r ela t ed (Ber n s, 1967; Gu a r d-F r ia r et al., 1986;
Ma cColl a n d Gu a r d-F r ia r, 1987). Am in o a cid sequ en ces est a blish ed fir m ly t h a t ext en sive h om ologies exist ed a m on g t h e va r iou s bilipr ot ein s. Sidler et
al. (1990) h a ve sh own fr om t h e a m in o a cid sequ en ce
of a cr ypt om on a d bilipr ot ein t h a t t h e b polypept ide
h a s a 73% h om ology t o t h e b polypept ide of r ed a lga l
B-ph ycoer yt h r in a n d a 63% h om ology t o cya n oba ct er ia l C-ph ycoer yt h r in . Cr ypt om on a ds, h owever, la ck
ph ycobilisom es (Ga n t t et al., 1971); t h eir bilipr ot ein s
a r e loca t ed in t h e in t r a t h yla koid spa ce, a n d t h ey
possess ch lor oph yll c in a ddit ion t o ch lor oph yll a.
Wh ile t h e b polypept ide of t h e cr ypt om on a d bilipr ot ein s is closely r ela t ed t o cya n oba ct er ia l a n d r ed
a lga e bilipr ot ein s (Sidler et al., 1990), t h e a polypept ide is of u n kn own or igin (Sidler, 1994). Sidler (1994)
r efer s t o t h e a m in o a cid sequ en ce of t h e cr ypt om on a d
a polypept ide a s t h e m ost in t r igu in g m yst er yin t h e
u n der st a n din g of bilipr ot ein ph ylogen y. An u n u su a l
N-m et h yla t ed a spa r a gin e r esidu e is con ser ved a n d
su ggest s a close r ela t ion sh ip a m on g a ll t h ese bilipr ot ein s (Wilba n ks et al., 1989). Cya n elles m igh t a lso be
der ived fr om cya n oba ct er ia l en dosym bion t s (e.g.,
Br ya n t et al., 1985; La m ber t et al., 1985).
Th e a m in o a cid sequ en ces of t h e bilipr ot ein s h a ve
been a n a lyzed for h om ologies (Apt et al., 1995;
Du cr et et al., 1994). P h ycoer yt h r ocya n in s belon g t o
t h e sa m e fa m ily a s t h e ph ycocya n in s. Th ey m a y be a
sepa r a t e gr ou p pla ced wit h in t h e ph ycocya n in
br a n ch . Du cr et et al. (1994) pr oposed t h a t ph ycoer yt h r ocya n in s a r e specia lized ph ycocya n in s a da pt ed for
gr een -ligh t a bsor pt ion .
Sch ir m er et al. (1985) discu ssed som e a spect s of
evolu t ion r ela t in g t o t h e x-r a y cr yst a llogr a ph ic st r u ct u r e of C-ph ycocya n in . Th e a- a n d b-polypept ides
h a ve ver y sim ila r t er t ia r y st r u ct u r es. In a ddit ion ,
ea ch polypept ide of C-ph ycocya n in h a s a r esem bla n ce t o t h e globin fold. P a r t s of globin pr ot ein s, like
m yoglobin , h a ve t er t ia r y st r u ct u r es sim ila r t o Cph ycocya n in . Th e a u t h or s su ggest ed t h a t C-ph ycocya n in a n d t h e globin s m a y h a ve evolved t o a sim ila r
st r u ct u r e fr om differ en t a n cest or s or m igh t h a ve
som e dist a n t r ela t ion sh ip.

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ROBE RT MACCOLL

Com plem en tary Ch rom atic Ad aptation

Th e a bilit y of ph ycobilisom es t o exh ibit va r ia bilit y
in t h e h a r vest in g of ligh t is m ost a dva n t a geou s in
a llowin g a good m a t ch bet ween t h e a bsor pt ion spect r a of a pa r t icu la r cya n oba ct er iu m a n d t h e a va ila ble
ligh t of it s h a bit a t . An exa m ple is a cya n oba ct er iu m
livin g on la n d a n d a n ot h er wh ich gr ows a t som e
dept h in t h e ocea n . Th e su n ligh t st r ikin g t h e ea r t h s
su r fa ce is br igh t a n d wh it e in color ; a s it m oves down
t h e wa t er colu m n t h e ligh t dim s a n d u su a lly becom es blu e-gr een . A cya n oba ct er iu m on la n d r equ ir es less ligh t h a r vest in g fr om it s ph ycobilisom es.
Typica lly, t h ey will h a ve t h e a lloph ycocya n in cor e
a n d r ods of C-ph ycocya n in , bu t per h a ps n o ph ycoer yt h r in . P h ycoer yt h r in s, h owever, a r e per fect ly su it ed
t o blu e-gr een ligh t a bsor pt ion a n d ext en d t h e a bilit y
of t h e cya n oba ct er iu m t o h a r vest m or e of a gr a du a lly
dim in ish in g ligh t a s it pr oceeds down t h e wa t er
colu m n . A ph ycobilisom e h a vin g C-ph ycoeyt h r in ,
C-ph ycocya n in , a n d a lloph ycocya n in will fill m ost
of t h e win dow of sm a ll ch lor oph yll a a bsor pt ion .
Th er efor e, m a r in e cya n oba ct er ia fr equ en t ly h a ve
ph ycobilisom es con t a in in g C-ph ycoer yt h r in or CUph ycoer yt h r in in t h eir r ods. Th e u r obilin s of CUph ycoer yt h r in s a r e excellen t a bsor ber s of blu e ligh t .
In a ddit ion t o a cya n oba ct er iu m seekin g a su it a ble
loca t ion for su ccessfu l gr owt h , som e cya n oba ct er ia

ca n a cclim a t e in va r iou s wa ys t o a r a n ge of h a bit a t s.

On e a cclim a t ion a va ila ble t o cer t a in cya n oba ct er ia is
com plem en t a r y ch r om a t ic a da pt a t ion . In t h is pr ocess, t h e r ods of t h e ph ycobilisom es ch a n ge t o a ch ieve
bet t er ligh t h a r vest in g in va r iou s cir cu m st a n ces.
Th e r ods a r e com posed of st a cked bilipr ot ein disks
(a6 b6 ), a n d t h e disk closest t o t h e cor e will a lwa ys be
ph ycocya n in . Th e r em a in in g disks ca n be eit h er
ph ycocya n in or ph ycoer yt h r in in m a n y com bin a t ion s.
Wh en a cya n oba ct er iu m exh ibit s com plem en t a r y
ch r om a t ic a da pt ion , t h e r ods of t h e ph ycobilisom es
ch a n ge wit h gr owt h ligh t (F ig. 5). Th e ch a n ge in clu des on e or bot h bilipr ot ein s a n d lin ker s (Ta n dea u
de Ma r sa c a n d Coh en -Ba zir e, 1977). Red gr owt h
ligh t m a y pr odu ce C-ph ycocya n in , wh ich a bsor bs r ed
well, a n d gr een gr owt h ligh t pr odu ces C-ph ycoer yt h r in , wh ich a bsor bs gr een well (F ig. 5). Th e key t o
t h is a da pt a t ion is t h e lin ker s t h a t va r y bet ween
27 000 a n d 36 000 m olecu la r m a ss. It wa s obser ved
h ow, for a pa r t icu la r cya n oba ct er iu m , t h e lin ker s
r espon ded t o gr owt h ligh t (F ig. 6). Rod lin ker s for
cya n oba ct er ia , except for cer t a in CU -ph ycoer yt h r in s, h a ve n o bilin s. F or r ed a lga e, lin ker s of
R-ph ycoer yt h r in s do h a ve bilin s.
Ma n y cya n oba ct er ia h a ve been st u died for t r en ds
in t h eir r espon ses t o com plem en t a r y ch r om a t ic a da p-

F IG. 5. Model for com plem en t a r y ch r om a t ic a da pt a t ion s of t wo cya n oba ct er ia . In on e ca se (A), C-ph ycocya n in in cr ea ses in r ed gr owt h
ligh t a n d in t h e ot h er (B), C-ph ycocya n in r em a in s con st a n t in va r yin g gr owt h ligh t . Ada pt ed fr om Siegelm a n a n d Kycia (1982) a n d
Gin gr ich et al. (1982a ).

P H YCOBILISOME S

F IG. 6. Th e dist r ibu t ion of lin ker s in ph ycobilisom es of a

pa r t icu la r cya n oba ct er iu m exh ibit in g com plem en t a r y ch r om a t ic
a da pt ion . L in dica t es lin ker, ba sed on t h e fin din gs of Zilin ska s a n d
H owell (1983).

t a t ion (Ta n dea u de Ma r sa c, 1977). Th r ee r espon ses

t o gr owt h ligh t a r e obser ved. No effect occu r s on t h e
r ods; m or e ph ycoer yt h r in is syn t h esized in gr een
gr owt h ligh t a n d less in r ed gr owt h ligh t , bu t Cph ycocya n in is in va r ia n t ; m or e ph ycoer yt h r in is
pr odu ced in gr een gr owt h ligh t a n d less in r ed
gr owt h ligh t , a n d C-ph ycocya n in is a lso ligh t con t r olled, bein g pr odu ced m or e in r ed t h a n in gr een
gr owt h ligh t (F igs. 5 a n d 6). It wou ld seem t h a t su ch
a h igh ly developed r espon se t o a ligh t h a bit a t m u st
be a n im por t a n t m ech a n ism for t h e su r viva l of
cya n oba ct er ia in sh ift in g en vir on m en t s. H owever,
t h er e a r e differ in g opin ion s (Sa ffo, 1987).
Sin ce t h e in it ia l obser va t ion (Ta n dea u de Ma r sa c
a n d Coh en -Ba zir e, 1977), lin ker s a n d com plem en t a r y ch r om a t ic a da pt ion h a ve been well in vest iga t ed
(Zilin ska s a n d H owell, 1983; Br ya n t , 1981, 1991;
Br ya n t a n d Coh en -Ba zir e, 1981; Ta n dea u de Ma rsa c, 1977, 1991; West er m a n n a n d Weh r m eyer, 1995;
Ta n dea u de Ma r sa c a n d H ou m a r d, 1993; Gla u ser et
al., 1992b; Gr ossm a n a n d Keh oe, 1997; Oh ki a n d
F u jit a , 1991, 1992; West er m a n n et al., 1993). A
specific lin ker is r equ ir ed for t h e a ddit ion of a
pa r t icu la r disk t o t h e r od. On e ph ycobilisom e lin ker,
L RC , is in va r ia n t sin ce it con n ect s t h e r od t o t h e cor e,
a n d t h e fir st disk in t h e r od is a lwa ys ph ycocya n in .
In gr een gr owt h ligh t , t h e n ext disk, L R , m igh t be a
C-ph ycoer yt h r in disk, wh ich wou ld r equ ir e syn t h esis of a com plet ely specific lin ker. At t a ch in g a secon d
C-ph ycoer yt h r in disk t o t h e fir st C-ph ycoer yt h r in
disk wou ld likewise r equ ir e syn t h esis of a n ot h er
u n iqu e lin ker. If gr owt h is t u r n ed t o r ed ligh t , t h e
specific lin ker s for a ddit ion of disks of C-ph ycoer yt h r in a r e n o lon ger syn t h esized a n d n ew lin ker s t h a t
ca n begin t o a dd C-ph ycocya n in disks m a y or m a y

319

n ot a ppea r. Aga in ea ch disk a dded t o t h e r od r equ ir es

a n ew a n d u n iqu e lin ker. E ffect s ot h er t h a n com plem en t a r y ch r om a t ic a da pt a t ion , e.g., r espon ses t o
ligh t in t en sit y, ca n a lso occu r in va r yin g t ypes of
gr owt h ligh t (F u jit a et al., 1994; Sidler, 1994).
A m a r in e cya n oba ct er iu m h a s pr ovided a u n iqu e
t ype of com plem en t a r y ch r om a t ic a da pt a t ion (West erm a n n a n d Weh r m eyer, 1995; West er m a n n et al.,
1993; Oh ki a n d F u jit a , 1992). In t h is cya n oba ct er iu m , r ed-ligh t gr owt h pr odu ced h em idiscoida l ph ycobilisom es a n d gr een ligh t r esu lt ed in h em iellipsoida l ph ycobilisom es. Th is ch a n ge in ph ycobilisom e
t ype occu r r ed t oget h er wit h t h e u su a l ch a n ge in
ph ycoer yt h r in a n d ph ycocya n in s in t h e r ods of t h ese
ph ycobilisom es. In a ll pr eviou s ca ses, com plem en t a r y ch r om a t ic a da pt a t ion s did n ot affect t h e h em idiscoida l st r u ct u r e.
Red a lga e a ppa r en t ly do n ot exh ibit com plem en t a r y ch r om a t ic a da pt a t ion (Ga n t t , 1990). Ga n t t (1990)
h a s r eviewed issu es of ph ot or egu la t ion s a s t h ey
per t a in t o t h e r ed a lga e, a s well a s cover in g im port a n t a spect s of t h eir bilipr ot ein s, ph ycobilisom es,
a n d ph ot osyn t h et ic a ct ivit ies. In t er m s of h ow r ed
a lga e r espon d t o ligh t (Ga n t t , 1990), it m igh t be
in t er est in g t o obser ve wh et h er t h e m a cr oph yt e r ed
a lga l sea weeds h a ve ver y differ en t m odes of a cclim a t ion wh en com pa r ed t o t h e u n icellu la r t ypes.
C-Ph ycocyan in an d Gen e Du plication
As discu ssed a bove, r ed ligh t ca n pr odu ce m or e
C-ph ycocya n in t o be a dded t o t h e r ods of cer t a in
cya n oba ct er ia . Br ya n t a n d Coh en -Ba zir e (1981) h a ve
st u died on e of t h ese cya n oba ct er ia a n d fou n d t h a t a
secon d set of a a n d b polypept ides of C-ph ycocya n in
wer e pr odu ced in r ed ligh t , in a ddit ion t o t h e u su a l a
a n d b polypept ides of t h is bilipr ot ein . Th e a m in o
a cid sequ en ces of t h e t wo C-ph ycocya n in s pr oved
t h a t t h e pr ot ein s wer e pr odu ct s of sepa r a t e gen es.
Ma zel a n d Ma r lie` r e (1989) gr ew a cya n oba ct er iu m
in a m ediu m con t a in in g m in im a l su lfu r. Th e u su a l
C-ph ycocya n in wa s r epla ced by a n ew C-ph ycocya n in h a vin g fewer su lfu r-con t a in in g a m in o a cids,
m et h ion in e a n d cyst ein e. As wit h cer t a in r ed-ligh t
gr own cya n oba ct er ia , ph ycoer yt h r in wa s elim in a t ed.
Th e r esu lt wa s a m or e efficien t u se of t h e sm a ll
a m ou n t of su lfu r a va ila ble. Th e bilin bin din g sit es
wer e n ot delet ed by t h is t h ir d t ype of C-ph ycocya n in
gen e.
R od L in k ers
Th e r oles of lin ker s in ca u sin g ph ycobilisom e r od
a ssem bly a n d spect r a l m odifica t ion s of bilipr ot ein s
h a ve a lr ea dy been pr esen t ed, bu t m or e det a ils ca n be
a dded. Lu n dell et al. (1981a ) pu r ified C-ph ycocya n in
a n d fou r lin ker s fr om a cya n oba ct er iu m . Th r ee of t h e
lin ker s (27 000, 30 000 a n d 33 000 Da ) a r e r od

320

ROBE RT MACCOLL

a ssocia t ed. E a ch lin ker wa s r ea ct ed wit h C-ph ycocya n in a s wer e m ixt u r es of lin ker s a n d t h e pr odu ct s
a n a lyzed. Th e 27 000-Da lin ker a n d C-ph ycocya n in
pr odu ced disks, a com plex of a6 b6 , a n d a 27 000-Da
lin ker. Th e 30 000- a n d 33 000-Da lin ker s, L R , beh a ved sim ila r ly, a n d t h ey cou ld pr odu ce bot h disks
(a6 b6 plu s on e lin ker ) a n d la r ge r od-like st r u ct u r es.
Th e disks cou ld be r ea dily pu r ified. It wa s est a blish ed t h a t t h e 27 000-Da lin ker, L RC , wa s a ssocia t ed
wit h t h e cor e, a n d t h er efor e, it s disk is t h e on e
im m edia t ely a dja cen t t o t h e cor e (Ya m a n a ka et al.,
1980; Lu n dell et al., 1981a ). Th is lin ker is specia l
sin ce it ser ves t o be in volved in r od t o cor e a ssem bly
a n d t o a dju st t h e spect r u m of C-ph ycocya n in t o h elp
t r a n sfer en er gy fr om r od t o cor e.
Th e fu n ct ion s of r od lin ker s h a ve a lso been st u died
by m et h ods ot h er t h a n com plem en t a r y ch r om a t ic
a da pt a t ion (Ya m a n a ka et al., 1980; Ya m a n a ka a n d
Gla zer, 1981; Willia m s et al., 1980; An der son et al.,
1984; Gin gr ich et al., 1982a ,b; de Lor im ier et al.,
1990b), a n d t h e fin din gs of t h ese st u dies su ppor t t h e
pr esen ce of a specific lin ker wit h ea ch disk a t a
pa r t icu la r r od loca t ion (Ta ble V).
Th er e is a 9000 m olecu la r m a ss lin ker, L 9R . It s
fu n ct ion is in volved wit h t er m in a t in g t h e len gt h of
r ods, a n d it m a y be com plexed wit h per iph er a l disks
(F u glist a ller et al., 1986; de Lor im ier et al., 1990a ,b).
CORE

Th e ph ycobilisom e cor e con t a in s lin ker s a n d t h e

a lloph ycocya n in s. Zilin ska s et al. (1978), Zilin ska s
(1982), Relin ger a n d Ga n t t (1981, 1982), a n d a ser ies
of defin it ive pa per s by Gla zer a n d co-wor ker s (e.g.,
Gla zer a n d Br ya n t , 1975; Gin gr ich et al., 1983;
Lu n dell a n d Gla zer, 1983a ,b,c; Lu n dell et al., 1981b;
Ya m a n a ka et al., 1982) pr odu ced t h e ba sis for a n
excellen t u n der st a n din g of t h is com plex a n d st r a t egica lly pla ced st r u ct u r e.
Two com pon en t s of t h e cor e possess low-en er gy
flu or escen ce sim ila r t o t h e ph ycobilisom e it self.
TAB LE V
Lin ker Assem bly F u n ct ion s
in a P a r t icu la r Cya n oba ct er iu m a
Lin ker
(m olecu la r m a ss)
27 000
33 500
31 500
30 500

F u n ct ion
J oin s C-ph ycocya n in disk t o cor e
J oin s secon d C-ph ycocya n in disk t o fir st
C-ph ycocya n in disk
J oin s fir st C-ph ycoer yt h r in disk t o secon d
C-ph ycocya n in disk
J oin s per iph er a l C-ph ycoer yt h r in disk t o
en d of r od

a In wh it e gr owt h ligh t , t h is cya n oba ct er iu m h a s ph ycobilisom e

r ods con sist in g of t wo C-ph ycocya n in disks a n d t wo C-ph ycoer yt h r in disks (Gin gr ich et al., 1982a ,b).

TAB LE VI
Cor e St r u ct u r es of H em idiscoida l P h ycobilisom es
Cylin der s a

Com posit ion

Bicylin dr ica l

Tr icylin dr ica l

A
B

P en t a cylin dr ica l

A
B
C

Bot h A cylin der s

a3 b3
a3 b3 L 8.9
c
a2 b2 b16 L cm
aB a2 b3 L 8.9
c
Sa m e a s bicylin dr ica l
a3 b3 (2 copies)
a3 b3 L 8.9
c (2 copies)
Sa m e a s bicylin dr ica l
Sa m e a s t r icylin dr ica l
Bot h C cylin der s
a3 b3 (1 copy)
a3 b3 L 8.9
c (1 copy)

Cor e t ype

a A r epr esen t s t wo ba sa l cylin der s, wh ich a r e a dja cen t t o

m em br a n e, B is t h e t op cylin der (F ig. 1), a n d C a r e per iph er a l
h a lf-cylin der s, wh ich a r e sit u a t ed on eit h er side of B.

Gla zer a n d Br ya n t (1975) isola t ed a com plex con t a in in g t h e aB a lloph ycocya n in -like polypept ide a n d n ot ed
t h a t it cou ld be t h e bilipr ot ein t o t r a n sfer en er gy t o
ch lor oph yll a. Th e a m in o a cid sequ en ce of aB is
kn own (Su t er et al., 1987). Th en fr om a r ed a lga
(Relin ger a n d Ga n t t , 1981) a n d fr om a cya n oba ct er iu m (Lu n dell et al., 1981b), la r ge m olecu la r m a ss
polypept ides of 95 000 a n d 75 000 Da , r espect ively,
wer e isola t ed. Bot h t h ese polypept ides (t h e a n ch or or
L cm polypept ides) h a d low-en er gy flu or escen ce sim ila r t o aB . So n ow, t h er e wer e t wo ca n dida t es for
en er gy m igr a t ion ou t of t h e ph ycobilisom e a n d in t o
t h e t h yla koid m em br a n e.
F or t h is r eview, it will be u sefu l t o focu s on a
pu blica t ion by Gin gr ich et al. (1983), a n d ot h er
pu blica t ion s sh ou ld be con su lt ed for m or e det a il
(Lu n dell a n d Gla zer, 1983a ,b,c; An der sen a n d E iserlin g, 1986; Du cr et et al., 1998). Th ese ph ycobilisom es
con t a in cor es of t h r ee cylin der s, t wo of wh ich a r e
a dja cen t t o t h e t h yla koid m em br a n e, t h e ba sa l cylin der s (F ig. 2). Th e cylin der n ot lyin g on t h e m em br a n e
su r fa ce, t h e t op cylin der, con t a in s fou r t r im er s of t h e
a lloph ycocya n in h a vin g a 650-n m m a xim u m , a n d
t h ese bilipr ot ein s r eceive en er gy fr om t h e r ods a n d
t r a n sfer it t o t h e lower-en er gy a lloph ycocya n in s.
E a ch of t h e t wo cylin der s on t h e t h yla koid su r fa ce
h a s t h e sa m e over a ll com posit ion : ea ch h a s t wo
t r im er s of a lloph ycocya n in (650 n m ) a n d t wo t r im er iclike st r u ct u r es ea ch in clu din g on e of t h e loweren er gy a lloph ycocya n in (Ta ble VI). Th e lower-en er gy
a lloph ycocya n in s a ppea r t o per for m t h e pivot a l r ole
of fu n n elin g en er gy ou t of t h e cor e a n d in t o t h e
t h yla koid m em br a n e t o ch lor oph yll a.
A 16.2- t o 18.3-kDa polypept ide, b16 , h a s been
isola t ed fr om t h e ph ycobilisom e cor es of cya n oba ct er ia (Ya m a n a ka et al., 1982; Lu n dell a n d Gla zer,
1983c; F u glist a ller et al., 1984; Ru m beli et al., 1987).

P H YCOBILISOME S

Th is polypept ide is a n ot h er bilipr ot ein a n d possesses

a sin gle ph ycocya n obilin . A color less lin ker is a lso
fou n d in t h e cor e. It s m olecu la r m a ss is 890010 500
da . It is design a t ed L 8.9
c , wh er e L in dica t es lin ker, c
m ea n s cor e, a n d 8.9 in dica t es kiloda lt on s. Th e effect
of t h is lin ker on t h e spect r u m of a lloph ycocya n in
t r im er s h a s been st u died (Bet z et al., 1993;
F u glist a ller et al., 1987; Got t sch a lk et al., 1993;
Lu n dell a n d Gla zer, 1983b; H olzwa r t h et al., 1990;
Sch n eider et al., 1995). An ot h er lin ker-r ela t ed polypept ide, wh ich is der ived fr om L cm , ca n a lso in du ce
spect r oscopic ch a n ges in a lloph ycocya n in (Got t sch a lk
et al., 1994).
Th e L cm lin ker is so n a m ed beca u se it is a ssocia t ed
wit h bot h t h e ph ycobilisom e cor e a n d t h e t h yla koid
m em br a n e. L cm is t h e la r gest polypept ide in t h e
ph ycobilisom es of cya n oba ct er ia a n d r ed a lga e a n d
m a y va r y in m olecu la r m a ss fr om a bou t 70 000 t o
128 000, depen din g on t h e sou r ce. It is m u lt ifu n ct ion a l h a vin g: (1) in volvem en t in t h e or ga n iza t ion of
t h e cor e; (2) a low-en er gy bilin t h a t pr oba bly is
r espon sible for en er gy t r a n sfer in t o t h e t h yla koid
m em br a n e; (3) t h e fu n ct ion of a n ch or in g t h e ph ycobilisom e cor e t o t h e t h yla koid m em br a n e; a n d (4) t h e
a bilit y t o m odify t h e spect r oscopic pr oper t ies of
a ssocia t ed bilipr ot ein (Ru sckowski a n d Zilin ska s,
1982; Redlin ger a n d Ga n t t , 1981, 1982; Ta n dea u de
Ma r sa c a n d Coh en -Ba zir e, 1977; Lu n dell a n d Gla zer,
1983a ,b,c; Lu n dell et al., 1981b; Mim u r o et al.,
1986b; Ga n t t et al., 1988; Ison o a n d Ka t oh , 1987;
Reu t er a n d Weh r m eyer, 1990; H ou m a r d et al., 1990;
Ga n t t , 1990; Ca pu a n o et al., 1991, 1993; Br ya n t ,
1991; Gin dt et al., 1992; Zh a o et al., 1992; Got t sch a lk
et al., 1994).
Th e L cm polypept ide h a s been loca t ed in bot h t h e
cor e of t h e ph ycobilisom e a n d t h e t h yla koid m em br a n e (Ta n dea u de Ma r sa c a n d Coh en -Ba zir e, 1977;
Redlin ger a n d Ga n t t , 1981, 1982; Ru skowski a n d
Zilin ska s, 1982) in bot h cya n oba ct er ia a n d r ed a lga e.
It is su ggest ed t h a t it fu n ct ion s by a t t a ch in g t h e
ph ycobilisom e cor e t o t h e t h yla koid m em br a n e. It is
r efer r ed t o a s t h e a n ch or polypept ide or t h e cor e
m em br a n e lin ker. St u dies on cya n oba ct er ia l ph ycobilisom es in dica t ed t h a t t h e L cm polypept ide m igh t
be t h e likely pa t h for t h e im por t a n t en er gy m igr a t ion
ou t of t h e ph ycobilisom e cor e a n d in t o t h e ph ot osyst em II r ecept or s (Mim u r o et al., 1986b). Th e r ole of aB
wa s su ggest ed t o be a bypa ss.
Ison o a n d Ka t oh (1987) discover ed a h em idiscoida l
ph ycobilisom e h a vin g a five-cyclin der cor e in a pa rt icu la r cya n oba ct er iu m . Th ey n ot ed t h a t t h e L cm
polypept ide fr om t h is cor e h a s a m olecu la r m a ss of
115 000, wh ich is gr ea t er t h a n t h a t fou n d in t wo or
t h r ee cylin der cor es. Wh en t h ey pr ot eolyt ica lly
clea ved a sm a ll piece fr om t h is L cm , t h e sm a ller L cm
pr odu ced a t r icylin dr ica l cor e. Ba sed on t h is decisive

321

discover y a n d ot h er da t a , t h ey pr oposed t h a t L cm wa s
st r on gly in volved in cor e a ssem bly. Th is a n a lysis
pr oved t o be ext r em ely in sigh t fu l.
It is kn own fr om it s a m in o a cid sequ en ce h ow L cm
ca n fill differ en t fu n ct ion s in t h e ph ycobilisom e cor e.
Br ya n t (1991) a n d Ca pu a n o et al. (1991) h a ve pr oposed m odels t h a t give L cm a pa r a m ou n t r ole in t h e
a ssem bly of t h e cor e. Th e a m in o a cid sequ en ces of
va r iou s L cm polypept ides a r e kn own ; see Sidler (1994)
for r efer en ces on bilipr ot ein a n d lin ker sequ en ces.
Br ya n t (1991) a n d Ca pu a n o et al. (1991) n ot e t h a t
t h e N-t er m in a l a m in o a cids r esem ble t h e sequ en ce of
a m in o a cids for t h e bilipr ot ein s a n d t h e bilin will be
loca t ed in t h is r egion . A loop, wh ich pr ot r u des fr om
t h is por t ion of t h e polypept ide, cou ld ser ve a s t h e
a n ch or of t h e ph ycobilisom e t o t h e t h yla koid m em br a n e. Th e r est of t h e sequ en ce is of t wo t ypes: a
r egion t h a t r esem bles t h e lin ker s of t h e ph ycobilisom e r ods, a n d a n ot h er r egion . Th e lin ker-like r egion is ca lled Rep a n d t h e ot h er Ar m . Th e Rep
r egion s a r e r epea t ed on ce for h em idisoida l ph ycobilisom es h a vin g a t wo-cylin der cor e a n d t wice for t h ose
wit h a t h r ee-cylin der cor e, h a vin g Ar m r egion s bet ween t h em . Th e pr oposa l is t h a t t h e Reps or ga n ize
t h e a lloph ycocya n in t r im er s t h e wa y t h e r od lin ker s
or ga n ize disks of ph ycocya n in , ph ycoer yt h r in , a n d
ph ycoer yt h r ocya n in . Th e Ar m s t wist a m on g t h e cor e
t o posit ion t h e Reps for t h is t a sk. Th e m olecu la r
m a ss of L cm in t h e t wo-cylin der cor es is a bou t 70 000
75 000 Da a n d for t h e t h r ee-cylin der cor es it is a bou t
92 00099 000 Da . E a ch Rep wou ld bin d t wo a lloph ycocya n in t r im er s. Th er e a r e t wo L cm polypept ides in
ea ch cor e, a n d, t h er efor e, for a t h r ee-cylin der cor e
t h e t wo L cm polypept ides wou ld h a ve six Rep dom a in s, wh ich cou ld bin d 12 t r im er s (F ig. 2). Ca pu a n o
et al. (1993) su ccessfu lly t est ed a spect s of t h is pr oposa l.
Th e t h ir d t ype of h em idiscoida l cor e h a s five
cylin der s. Th r ee of t h e cylin der s a r e t h e sa m e in
com posit ion a n d loca t ion a s t h e t h r ee-cylin der cor es.
Th e r em a in in g t wo a r e h a lf-cylin der s a n d a r e com posed of a lloph ycocya n in t r im er s, a3 b3 L 8.9
c a n d a 3 b3 .
Th ey a r e loca t ed a bove t h e t wo ba sa l cylin der s t h a t
a r e con t igu ou s t o t h e t h yla koid m em br a n e a n d on
eit h er side of t h e t op cylin der (Sidler, 1994). Th e L cm
polypept ide is a bou t 115 000 t o 128 000 Da a n d h a s
fou r Rep dom a in s. Th e fou r t h Rep m a y fu n ct ion t o
or ga n ize t h e t wo-h a lf cylin der s, ca lled t h e C or
per iph er a l cylin der s, of t h e cor e. Th e t wo L cm polypept ides in t h is cor e wou ld t ot a l eigh t Reps a n d cou ld
posit ion t h e 16 t r im er s. Du cr et et al. (1996, 1998)
h a ve st u died pen t a cylin dr ica l a lloph ycocya n in cor es
in det a il a n d h a ve pr esen t ed m u ch eviden ce con cer n in g t h eir st r u ct u r e. Th ey pr opose t h a t t h e r ods a r e
a t t a ch ed t o t h e cor e a s follows: t h e ba sa l cor e cylin der s a dja cen t t o t h e t h yla koid m em br a n e h a ve on e

322

ROBE RT MACCOLL

r od a t t a ch ed t o ea ch , a n d t h e t op cylin der a n d t wo
per iph er a l h a lf-cylin der s bin d t wo r ods ea ch .
Cya n oba ct er ia l m u t a n t s t h a t la ck ph ycobilisom e
r ods h a ve been con st r u ct ed (Br ya n t , 1991; Bh a ler a o
et al., 1995; An der son et al., 1984). Th e or ga n ism s
st ill possess fu n ct ion a l a lloph ycocya n in cor es.
Ph ycobilisom es an d Ph otosystem I
Th e a ssocia t ion of ph ycobilisom es t o ph ot osyst em
II is qu it e st r on g, a n d com plexes of t h e t wo h a ve
been isola t ed a n d st u died (Clem en t -Met r a l et al.,
1985; Ch er eskin et al., 1985). It h a s been lon g kn own
t h a t u n der cer t a in gr owt h -ligh t con dit ion s t h a t en er gy a bsor bed by t h e ph ycobilisom es cou ld be u sed
by ph ot osyst em I, bu t on ly r ecen t ly h a s it becom e
a ppa r en t t h a t ph ycobilisom es cou ld dir ect ly t r a n sfer
en er gy t o ph ot osyst em I. St u dies on a wild-t ype a n d
a m u t a n t of a cya n oba ct er iu m yielded da t a con sist en t wit h dir ect t r a n sfer of en er gy fr om t h e ph ycobilisom es t o ph ot osyst em I (Mu llin ea u x 1992, 1994). In
a m u t a n t la ckin g ph ot osyst em II, ph ycobilisom es
t r a n sfer r ed excit a t ion en er gy t o ph ot osyst em I (Mu llin ea u x, 1994).
Usin g m u t a n t s of aB a n d L cm , it wa s dem on st r a t ed
(Ma xson et al., 1989; Br ya n t , 1991; Zh a o et al., 1992;
Gin dt et al., 1992) t h a t t h e L cm polypept ide a lon e is
su fficien t t o m edia t e ext en sive en er gy m igr a t ion t o
ph ot osyst em II. Addit ion a l r esu lt s st r on gly in dica t ed
t h a t a fu n da m en t a l r ole of aB is en er gy t r a n sfer t o
ph ot osyst em I. Th e aB dir ect ion of excit a t ion en er gy
t o ph ot osyst em I wou ld occu r u n der gr owt h ligh t
t h a t st r on gly fa vor ed ph ot osyst em II.
An en zym e, fer r edoxin -NADP 1 oxidor edu ct a se, is
fou n d t o h a ve a n N-t er m in a l a m in o a cid sequ en ce
t h a t is 78% sim ila r t o t h e r od-t er m in a t in g lin ker, L 9R .
It is, t h er efor e, specu la t ed t h a t t h e en zym e, for
wh ich t h er e is eviden ce of ph ycobilisom e a ssocia t ion ,
cou ld bin d t o a ph ycobilisom e r od a t t h e disk fu r t h est
fr om t h e cor e (Sch u ch t er a n d Br ya n t , 1992). Th is
obser va t ion su ggest s t h a t ph ycobilisom es ser ve a
fu n ct ion in pr ovidin g m olecu les wit h a ccess t o t h e
t h yla koid m em br a n e su r fa ce. In pa r t icu la r, t h is en zym e sh ou ld be a ssocia t ed wit h ph ot osyst em I.
Ba ld et al. (1996) a n d Sidler (1994) h a ve ext en sively r eviewed t h e det a ils of t h e in t er a ct ion a m on g
ph ycobilisom es a n d r ecept or s in t h e t h yla koid m em br a n e. P h ycobilisom es pr im a r ily t r a n sfer excit a t ion
en er gy t o ph ot osyst em II r ecept or s, bu t u n der cert a in ligh t con dit ion s dir ect t r a n sfer t o ph ot osyst em I
m a y occu r. Act u a l dockin g of ph ycobilisom es t o ph ot osyst em I is discu ssed (Ba ld et al., 1996). Dockin g
m igh t be a ccom plish ed t h r ou gh t h e aB -con t a in in g
cor e t r im er, by fer r edoxin -NADP 1 oxidor edu ct a se, or
by som e ot h er m ech a n ism . F u jit a et al. (1994) h a s
r eviewed t h e ca ses for a n d a ga in st dir ect t r a n sfer of

excit a t ion en er gy t o ph ot osyst em I fr om t h e ph ycobilisom es.

A cya n oba ct er ia l m u t a n t t h a t h a s n o ph ycobilisom e cor e h a s been pr epa r ed (Su et al., 1992). Th e
ph ycocya n in a ggr ega t es t h a t wer e pr esen t t r a n sfer r ed t h eir en er gy pr im a r ily a n d dir ect ly t o ph ot osyst em I.
EN ERGY TRAN S F ER B ETWEEN B ILIN S

It h a s been sh own t h a t a bsor bed en er gy m igr a t es

t h r ou gh t h e r ods in t o t h e cor e a n d t h en t o t h e
ch lor oph yll a in t h e t h yla koid m em br a n e. Th ese
even t s a r e n on r a dia t ive, ver y efficien t , a n d dir ect ion a l. Met h ods h a ve been em ployed, pa r t icu la r ly for
lin ker-fr ee C-ph ycocya n in , ph ycoer yt h r ocya n in , a n d
a lloph ycocya n in (650-n m m a xim u m ), t o develop a n
u n der st a n din g of t h e in dividu a l st eps in t h is com plex pr ocess. Th ese a ppr oa ch es a r e ba sed on t h e
a n a lysis of da t a obt a in ed by fa st la ser kin et ics a n d
x-r a y diffr a ct ion st u dies on cr yst a ls t oget h er wit h
va r iou s opt ica l spect r a . Th e a r ch it ect u r e of t h e ph ycobilisom e a n d t h e or ga n iza t ion of it s m a n y bilin s
pr ovides efficien t en er gy m igr a t ion fr om t h e h igh est en er gy bilin t o t h e lowest , fr om wh ich en er gy is
t r a n sfer r ed t o ch lor oph yll a. It st ill n eeds t o be
u n der st ood h ow t h e bilin or ga n iza t ion est a blish es
t h is efficien cy.
Cr yst a ls for va r iou s cya n oba ct er ia l bilipr ot ein s
h a ve been pr epa r ed by H u ber a n d co-wor ker s a n d
su bject ed t o x-r a y diffr a ct ion a n a lysis (Sch ir m er et
al., 1985, 1986, 1987; Br ejc et al., 1995; Du er r in g et
al., 1990, 1991). All t h e t r im er ic a n d h exa m er ic
bilipr ot ein s h a ve ver y sim ila r gen er a l st r u ct u r es
(F ig. 7). Th e cen t r a l ch a n n el is com m on in a ll ca ses,
h a vin g a 3.5- t o 4.5-n m dia m et er. Cer t a in of t h e
bilin s (b84) a r e in close pr oxim it y t o t h is open in g.
Bot h polypept ides h a ve n in e a-h elices con n ect ed by
ir r egu la r t u r n s a n d h a ve sim ila r t er t ia r y st r u ct u r es.
Alloph ycocya n in wh en pu r ified is com posed of t h r ee
pr ot ein m on om er (ab) u n it s. E a ch a a n d ea ch b
polypept ide h a s on e ph ycocya n obilin . Th e t wo closest bilin s (a84 a n d b84) a r e on a dja cen t m on om er s
20.6 n m a pa r t , wh ile bilin s on t h e sa m e m on om er a r e
49.6 n m a pa r t (F ig. 8). Th ese dist a n ces m igh t in dica t e t h a t t h e en er gy t r a n sfer even t s differ sh a r ply
for m on om er s a n d t r im er s. F or C-ph ycocya n in , m on om er s, t r im er s, h exa m er s, a n d r od a ssem blies h a ve
been st u died by x-r a y cr yst a llogr a ph y. Th e dist a n ces
bet ween t h e a84 a n d t h e b84 bilin s of C-ph ycocya n in
m on om er s a n d t r im er s (F ig. 9) ch a n ge in r ela t ive
posit ion a s fou n d for a lloph ycocya n in .
H ow is en er gy t r a n sfer r ed in ph ot osyn t h esis? Th er e
is a ppa r en t ly on e pr edom in a t e m ech a n ism , F or st er
r eson a n ce t r a n sfer in t h e wea k cou plin g lim it (F orst er, 1965), t h a t pr ovides m u ch of t h e ch r om oph or et o-ch r om oph or e t r a n sfer. In t h is m et h od, som et im es

P H YCOBILISOME S

323

F IG. 9. Rela t ive bilin a r r a n gem en t in C-ph ycocya n in t r im er s.

Th e pr efix is t h e n u m ber of t h e m on om er, a n d t h e su ffix is t h e
posit ion in t h e a m in o a cid sequ en ce of t h e cyst ein e t o wh ich a bilin
is a t t a ch ed. Th e a r r ow lin ks t h e t wo bilin s t h a t a r e closest a n d
m ost st r on gly cou pled.

F IG. 7. Dia gr a m of t h e x-r a y diffr a ct ion r esu lt s for a lloph ycocya n in t r im er. Th e gen er a l sh a pe a n d cen t r a l ch a n n el a r e sim ila r
for a ll t h e bilipr ot ein s st u died so fa r a s t r im er s a n d h exa m er s
fr om ph ycobilisom es. Bilin loca t ion s a r e in dica t ed by a r r ows. Th e
n u m ber s 1, 2, a n d 3 r efer t o t h e t h r ee m on om er ic u n it s. E a ch
m on om on er is com posed of a n a (ligh t ) a n d a b (da r k) polypept ide.
Th e b84 bilin s a r e poin t in g in t o t h e cen t r a l ch a n n el, a n d t h e a84
bilin s a r e loca t ed on t h e per iph en y of t h e st r u ct u r e.

ca lled ver y wea k dipoledipole cou plin g, t h e in dividu a l ch r om oph or es t en d t o r et a in t h eir spect r a . A
secon d m ech a n ism , excit on cou plin g, m a y occu r wh en
ch r om oph or es a r e br ou gh t in t o closer con t a ct (Ca n t or a n d Sch im m el, 1980). In t h is m et h od, a pa ir of
ch r om oph or es m a y sh a r e deloca lized en er gy, beh a vin g a s if t h ey a r e on e u n it . In excit on cou plin g, t h e
excit ed st a t es of t h e in dividu a l ch r om oph or es a r e
split in t o h igh a n d low en er gies (F ig. 10). In t er n a l
con ver sion pr ovides for t h e m ovem en t of en er gy fr om

t h e h igh - t o low-en er gy st a t es of t h e cou pled ch r om oph or e pa ir. Th is sit u a t ion m a y be obser ved by a sh ift
in a bsor pt ion m a xim u m .
C-Ph ycocyan in
Th e en er gy m igr a t ion pr ocess for isola t ed bilipr ot ein s wa s fir st a n a lyzed by Da le a n d Tea le (1970) a n d
Tea le a n d Da le (1970) u sin g flu or escen ce pola r iza t ion . Sin ce t h en m a n y st u dies h a ve been ca r r ied ou t
on t h is t opic. F or C-ph ycocya n in , t h e m or e r ecen t
r esu lt s will be discu ssed in wh ich x-r a y cr yst a llogr a ph y da t a , fem t osecon d la ser r esu lt s, a n d t h e m ost
soph ist ica t ed spect r a l decon volu t ion s wer e em ployed.
Debr eczen y et al. (1993, 1995a , 1995b) h a ve a n a lyzed t h e en er gy t r a n sfer pr oper t ies of C-ph ycocya n in m on om er s a n d t r im er s a n d det er m in ed t h a t
F or st er r eson a n ce en er gy t r a n sfer is t h e m et h od
u sed for t h e r a dia t ion less t r a n sfer of en er gy bet ween
t h e va r iou s pa ir s of bilin s on t h ese t wo oligom er s. A

F IG. 8. Rela t ive bilin a r r a n gem en t for a lloph ycocya n in t r im er s. Th e pr efix is t h e n u m ber of t h e m on om er, a n d t h e su ffix (st r u ct u r e on
t h e r igh t ) is t h e posit ion in t h e a m in o a cid sequ en ce of t h e cyst ein e t o wh ich a bilin is a t t a ch ed.

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ROBE RT MACCOLL

F IG. 10. Dia gr a m of en er gy levels for a ch r om oph or e dim er

in volved in excit on cou plin g. Ar r ow poin t s t o in cr ea sin g en er gy.

m u t a n t of C-ph ycocya n in wa s u sed ext en sively in

wh ich t h e b155 cyst ein e wa s r epla ced by a ser in e.
Th e r esu lt in g bilipr ot ein h a d bilin s a t b84 a n d a84,
bu t of cou r se n ot a t b155. Usin g t h e m u t a n t a n d
wild-t ype pr ot ein s, t h e a bsor pt ion a n d flu or escen ce
spect r a of t h e t h r ee bilin s wer e det er m in ed (Ta ble
IV). Th ese spect r a a r e n ecessa r y beca u se in F or st er
r eson a n ce t h eor y t h e m odified spect r a l over la p bet ween t h e flu or escen ce of t h e don or a n d t h e a bsor pt ion of t h e a ccept or is key da t a . F r om t h ese r esu lt s,
ot h er spect r a l da t a , t h e r efr a ct ive in dex, a n d t h e
dist a n ce a n d or ien t a t ion s of t h e bilin s fr om x-r a y
cr yst a llogr a ph y (Sch ir m er et al., 1987; Du er r in g et
al., 1990, 1991), t h ey det er m in ed, u sin g F or st er
t h eor y, t h e r a t e con st a n t s for en er gy t r a n sfer for t h e
va r iou s bilin pa ir s. F or m on om er, en er gy t r a n sfer s
fr om b155 t o b84 a n d a84 t o b84 wer e fou n d t o occu r
r a pidly (Ta ble VII). Th e F or st er-ca lcu la t ed va lu es
a gr eed well wit h t h e exper im en t a l r esu lt s. Rela t ively slow en er gy t r a n sfer wa s fou n d for t h e t r a n sfer fr om b155 t o a84, a n d t h is lifet im e wa s pr odu ced
by t h e u n fa vor a ble or ien t a t ion of t h ese bilin s. Th e
r a dia t ive flu or escen ce lifet im es for t h ese bilin s a r e
a bou t 12 n s, a n d n on r a dia t ive pr odu ct ive en er gy
t r a n sfer m u st be m u ch fa st er. Th e b84 bilin is t h e
lowest -en er gy bilin in t h e m on om er s a n d will ser ve
a s t h e bilin fr om wh ich en er gy is t r a n sfer r ed ou t of
t h e pr ot ein . Th e ot h er t wo h igh er-en er gy bilin s, b155
a n d a84, ext en d t h e r a n ge of ligh t h a r vest in g. Th e
b155 bilin a bsor bs a t t h e h igh est en er gy.
F or t r im er s (in t h e a bsen ce of lin ker s), t h er e a r e
m or e possibilit ies for en er gy t r a n sfer, especia lly
TAB LE VII
E n er gy Tr a n sfer bet ween P a ir s of Bilin s in
C-P h ycocya n in Mon om er s

Bilin pa ir
b155 t o a84
b155 t o b84
a84 t o b84
a

Dist a n ce Or ien t a t ion

()
(degr ees)
48.0
34.2
50.5

62
47
16

Debr eczen y et al. (1995a ).

E xper im en t a l a Ca lcu la t ed
en er gy
en er gy
t r a n sfer (ps) t r a n sfer (ps) a
.500
52
149

815890
4649
111158

bet ween t h e closely spa ced a84 a n d b84 bilin s on

con t igu ou s pr ot ein m on om er s in t h e t r im er (F ig. 9).
A deca y t im e of 1.0 ps wa s ca lcu la t ed fr om t h e
F or st er r a t e con st a n t for t h is in t er m on om er ic t r a n sfer. Th e exper im en t a l r esu lt for t r a n sfer bet ween
t h is pa ir of bilin s wa s 1.4 ps, wh ich a gr eed ver y
n icely wit h t h e F or st er ca lcu la t ion s in t h e wea k
cou plin g lim it . F or t h e in t r a m on om er ic t r a n sfer fr om
b155 t o b84, t h e F or st er ca lcu la t ion ga ve 49 ps. Th e
a u t h or s su ggest ed t h a t t h ese r esu lt s wer e t h e fir st
det a iled eviden ce for F or st er r eson a n ce en er gy t r a n sfer bet ween ch r om oph or es on a pr ot ein .
Ot h er gr ou ps u sin g C-ph ycocya n in t r im er s h a ve
a lso exper im en t a lly st u died en er gy t r a n sfer fr om
a84 t o b84 (Gillbr o et al., 1993; Xie et al., 1992).
Gillbr o et al. (1993) fou n d a 500-fs en er gy t r a n sfer
a n d su ggest ed t h e r esu lt s su ppor t F or st er r eson a n ce
t r a n sfer. Xie et al. (1992), h owever, r epor t ed t h a t
t h eir r esu lt s wer e in con sist en t wit h F or st er in du ct ive r eson a n ce en er gy t r a n sfer t h eor y. Th is con clu sion wa s ba sed on a n a n a lysis of t h e wa velen gt h
depen den ce of t h e flu or escen ce depola r iza t ion kin et ics.
Less is kn own a bou t en er gy m igr a t ion wit h in
h exa m er s a n d bet ween h exa m er s of C-ph ycocya n in .
Wh en h exa m er s for m , n ew pa t h wa ys for en er gy
m igr a t ion a r e open ed (Sch ir m er et al., 1986; Du err in g et al., 1991). F or efficien t en er gy t r a n sfer bet ween h exa m er s, t h e cr yst a l st r u ct u r es su ggest t h a t
t h e b84 bilin s pr ovide t h e pa t h wa ys.
Dem idov a n d co-wor ker s h a ve pr odu ced in sigh t s
on en er gy t r a n sfer, flu or escen ce pola r iza t ion , a n d
decon volu t ion of spect r a for C-ph ycocya n in (Dem idov a n d Mim u r o, 1995; Dem idov a n d An dr ews, 1995;
Dem idov a n d Bor isov, 1993, 1994; Dem idov, 1994a ,b).
Th e m on om er a bsor pt ion spect r u m of C-ph ycocya n in
wa s decon volu t ed u sin g a pr ocedu r e in volvin g t h eir
t h eor et ica l t r ea t m en t of spect r a (Ta ble IV). Aft er t h e
t wo bilin s on t h e b polypept ide wer e r esolved, t h e a
polypept ide spect r u m wa s a dded, a n d t h e flu or escen ce, flu or escen ce pola r iza t ion , a n d flu or escen ce
qu a n t u m yield of t h e m on om er wer e est im a t ed. Th e
ca lcu la t ed a n d exper im en t a l spect r a sh owed a ccept a ble a gr eem en t s (Dem idov a n d Mim u r o, 1995). Th er e
wer e a lso ea r lier st u dies on ch r om oph or e a ssign m en t s in C-ph ycocya n in (Siebzeh n r u bl et al., 1987;
Mim u r o et al., 1986a ).
Dem idov a n d Mim u r o (1995) n ot ed t h a t t h eir
decon volu t on of t h e m on om er C-ph ycocya n in a bsor pt ion spect r u m differ ed by 46 n m (Ta ble IV) fr om
t h ose obt a in ed by Debr eczen y et al. (1993). Th ey
su ggest ed t h ese r esu lt s cou ld be expla in ed by t h e
fa ct t h a t t h e C-ph ycocya n in u sed in t h e t wo st u dies
ca m e fr om differ en t cya n oba ct er ia . Th is idea m a y
h a ve m er it . C-P h ycocya n in , isola t ed fr om a pa r t icu la r t h er m oph ilic cya n oba ct er iu m , h a d a sign ifica n t ly

P H YCOBILISOME S

blu e-sh ift ed a bsor pt ion spect r u m com pa r ed t o ot h er

C-ph ycocya n in s (E dwa r ds et al., 1996). Mon om er s
h a d a n a bsor pt ion m a xim u m a t 608 n m com pa r ed t o
ot h er m on om er s a t a bou t 614 n m . It wa s pr oposed
t h a t on e or m or e ph ycocya n obilin s on t h is pr ot ein
wer e a ffect ed differ en t ly by a popr ot ein t h a n for ot h er
C-ph ycocya n in s. Sch n eider et al. (1993), a lso, fou n d
spect r oscopic differ en ces a m on g t r im er s of C-ph ycocya n in s fr om differ en t cya n oba ct er ia .
Ph ycoeryth rocyan in
P h ycoer yt h r ocya n in is fou n d in cer t a in cya n oba ct er ia , wh ich la ck ph ycoer yt h r in . It s a m in o a cid sequ en ce (F u gist a ller et al., 1983) a n d t h r ee-dim en sion a l st r u ct u r e (Du er r in g et al., 1990) a r e kn own .
Like C-ph ycocya n in it h a s t h r ee bilin s per m on om er
a t a84, b84, a n d b155 (Ta ble III). It s u n iqu en ess is in
it s bilin a t a84, wh er e it possesses a ph ycoviolobilin .
P a r bel et al. (1997) h a ve sh own t h a t t h e b84 ph ycocya n obilin is a t t h e lowest en er gy a n d t h e ph ycoviolobilin is t h e h igh est -en er gy bilin . In t h is st u dy, t h e
opt ica l spect r a of t h e in dividu a l polypept ides, m on om er s, a n d t r im er s wer e obt a in ed. Mon om er s a n d
t r im er s h a d differ en ces in t h eir spect r a , a n d excit on ic cou plin g bet ween a dja cen t m on om er s of t h e
t r im er wa s discu ssed. F em t osecon d a bsor pt ion st u dies h a ve been ca r r ied ou t on t h is bilipr ot ein (H u cke
et al., 1993).
Alloph ycocyan in
E a r ly on , t h er e wer e t wo pr oposa ls t o expla in wh y
a lloph ycocya n in t r im er s wou ld h a ve a 650-n m m a xim u m a n d C-ph ycocya n in t r im er s h a ve t h eir a bsor pt ion m a xim u m a t 621 n m . On e su ggest ion wa s t h a t
on e of t h e bilin s on a lloph ycocya n in t r im er s wou ld
exper ien ce a differ en t a popr ot ein in t er a ct ion (Mu r a ka m i et al., 1981). Th e ot h er wa s t h a t a lloph ycocya n in t r im er s m igh t h a ve t wo in t er a ct in g bilin s, wit h
close pr oxim it y on a dja cen t m on om er s t h a t pr odu ced
t h e r ela t ively sh a r p 650-n m a bsor pt ion m a xim u m
(Csa t or da y et al., 1984; H u a n g et al., 1987; Ma cColl
et al., 1980). In con t r a st , t h e m on om er (ab) spect r a of
a lloph ycocya n in a n d C-ph ycocya n in a r e sim ila r (Ma cColl et al., 1980; Mu r a ka m i et al., 1981).
Th e differ en ce bet ween t h e a bsor pt ion spect r a of
m on om er s a n d t r im er s of a lloph ycocya n in is st r ikin g, a n d it wa s t h ou gh t t h is ch a n ge m igh t a llow a
st u dy of t h e u n u su a l 650-n m m a xim u m of t r im er s.
H om ogen ou s m on om er s for a lloph ycocya n in wer e
fou n d t o h a ve a n a bsor pt ion m a xim u m a t 614 n m ,
wh ile t r im er s h a d a sh a r p m a xim u m a t 650 n m a n d a
pr om in en t sh ou lder a t a bou t 610620 n m . Th e flu or escen ce (excit a t ion ) pola r iza t ion spect r a of m on om er s a n d dim er s wer e likewise differ en t (Ma cColl et
al., 1980). Th e t r im er spect r u m h a d a pola r iza t ion of
10.05, wh ile m on om er s a ppr oa ch ed 10.4 a t t h e r ed

325

edge. Th er e h a ve been t wo qu it e differ en t pr oposa ls

t o expla in t h e spect r oscopic differ en ces. In on e ca se,
on e of t h e bilin s on t h e m on om er, eit h er a84 or b84,
is ch a n ged by in t er a ct ion wit h a popr ot ein wh en
t r im er s a r e for m ed. Th e ch a n ged bilin t h en possesses t h e 650-n m m a xim u m . Th e bilin m igh t h a ve a
u n iqu e con for m a t ion (Su gim ot o et al., 1984), or be in
a differ en t en vir on m en t . Th e ot h er bilin r et a in s a
spect r u m sim ila r t o wh a t it h a d in t h e pr ot ein
m on om er, a n d it n ow a ppea r s a s t h e 610- t o 620-n m
sh ou lder in t h e t r im er spect r u m . E n er gy t r a n sfer in
t h is scen a r io wou ld be by F or st er r eson a n ce fr om on e
in dividu a l don or bilin a t 610620 n m t o t h e secon d
a ccept or bilin a t 650 n m . Sch n eider et al. (1995)
r eviewed det a ils of h ow t h e en er gy levels cou ld be
a ffect ed fr om m on om er t o t r im er a n d t o t r im er wit h
lin ker. Th e secon d pr oposa l su ggest ed t h a t t h e bilin s
m igh t be close t oget h er a n d pr oper ly or ien t ed in t h e
t r im er oligom er a cr oss t h e m on om er m on om er in t erfa ce. Th ese bilin s wou ld en ga ge in excit on split t in g
a n d t h e t wo bilin s, a84 a n d b84, wou ld sh a r e excit a t ion deloca liza t ion . Th e 650-n m m a xim u m a n d 610t o 620-n m sh ou lder wou ld be t h e t wo excit on st a t es.
In st ea d of F or st er r eson a n ce t r a n sfer, in t h is m odel
in t er excit on -st a t e r ela xa t ion wou ld a llow t h e t r a n sfer of en er gy.
St u dies on t h e m on om er t r im er equ ilibr iu m wer e
ca r r ied ou t u sin g kin et ics t ech n iqu es (H u a n g et al.,
1987). Wh en t h e ch a n ge fr om t r im er s t o m on om er s
wa s st u died u sin g ligh t sca t t er in g, a sin gle expon en t ia l deca y wa s obser ved. Sin ce ligh t sca t t er in g m ea su r es t h e ch a n ges in m olecu la r m a ss, t h is r esu lt wa s
a dir ect m ea su r e of t h e ch a n ge fr om t r im er s t o
m on om er s. Th e iden t ica l exper im en t wa s a lso perfor m ed u sin g a bsor pt ion ch a n ges a s t h e m on it or in g
m et h od. In t h is ca se, t h er e wer e t wo even t s. Th e
fa st er wa s n ea r ly sim u lt a n eou s wit h t h e ligh t sca t t erin g kin et ics, a n d t h e secon d a bsor pt ion ch a n ge wa s
m u ch slower. Th e fa st er ch a n ge wou ld be expect ed in
t h e ca se of excit on cou plin g sin ce t h e pa ir of bilin s on
t r im er s wou ld lose t h eir split spect r u m a t t h e sa m e
r a t e t h a t m on om er s wer e for m ed. Th e slower ch a n ge
cou ld be a ch a n ge in t h e bilin s a s n ewly for m ed
a lloph ycocya n in m on om er s r ea r r a n ged t o for m t h eir
m ost st a ble t er t ia r y a n d secon da r y st r u ct u r es. Th is
r esu lt su ggest s t h a t bot h fa ct or sexcit on split t in g
a n d bilin en vir on m en t or con for m a t ion con t r ibu t e
t o spect r oscopic differ en ces bet ween m on om er s a n d
t r im er s, bu t t en t a t ively poin t s t o excit on split t in g a s
est a blish in g t h e en er gy t r a n sfer m ech a n ism in t r im er s.
Th e x-r a y cr yst a llogr a ph y r esu lt s on a lloph ycocya n in t r im er s (Br ejc et al., 1995) sh ow t h a t t h er e seem s
t o be a bilin wit h a n u n u su a l con for m a t ion , bu t t h ey
a lso sh ow a som ewh a t sm a ll dist a n ce bet ween bilin s
on a dja cen t m on om er ic u n it s (F ig. 8). Br ejc et al.

326

ROBE RT MACCOLL

(1995) fa vor t h e for m er fa ct or for t h e ca u se of t h e

650-n m a bsor pt ion m a xim u m . It wou ld be of in t er est
for a t h eor et ica l a n a lysis t o be per for m ed on t h is
bilin con for m a t ion t o det er m in e wh et h er it wou ld
gen er a t e t h e 650-n m a bsor pt ion m a xim u m .
F a st la ser kin et ics st u dies (H om oelle et al., 1998;
Sh a r kov et al., 1992, 1994; E din gt on et al., 1995,
1996; Gillbr o et al., 1993; Xie et al., 1992) h a ve n ot
yielded a con sen su s decision on h ow en er gy is t r a n sfer r ed bet ween t h e t wo closest bilin s of a lloph ycocya n in t r im er s. Som e da t a a ppea r t o st r on gly fa vor t h e
idea t h a t t wo in depen den t bilin s h a vin g differ en t
spect r a t r a n sfer en er gy fr om t h e h igh -en er gy t o
low-en er gy bilin by t h e F or st er r eson a n ce m ech a n ism . Ot h er da t a in dica t e a ver y differ en t m ech a n ism : t h a t t h is pa ir of bilin s a r e su fficien t ly close
t oget h er a n d sh a r e deloca liza t ion en er gy.
Sh a r kov et al. (1992) u sed a fem t osecon d a bsor pt ion m et h od a n d fou n d a 440-fs (0.44 ps) lifet im e
h a vin g a 0.4 a n isot r opy du r in g t h e fir st few picosecon ds. Th ey pr opose t h a t t h ese r esu lt s su ppor t a
m odel of a n a lloph ycocya n in t r im er in wh ich t h er e
a r e t wo u n cou pled bilin s, h a vin g m a xim a a t 600 or
650 n m . E n er gy is t r a n sfer r ed fr om t h e 600-n m bilin
t o t h e 650-n m bilin by t h e F or st er r eson a n ce m ech a n ism . Sh a r kov et al. (1994) likewise fou n d a gr eem en t bet ween t h eir fem t osecon d spect r oscopy da t a
a n d F or st er r eson a n ce t r a n sfer.
In con t r a st , E din gt on et al. (1995) fou n d t wo-color
pu m p pr obe exper im en t s on a lloph ycocya n in t r im er s
ga ve a n in it ia l a n isot r opy of 0.580.70. Th ey n ot ed
t h a t a n isola t ed dipole wou ld h a ve a m a xim u m
a n isot r opy of 0.4, bu t a cou pled pa ir of ch r om oph or es
cou ld h a ve a va lu e u p t o 0.7. In a ddit ion , t h ey fou n d
a fa st est deca y com pon en t of 1030 fs a n d m a in t a in
t h a t t h is is t oo sh or t for F or st er r eson a n ce en er gy
t r a n sfer. Th eir da t a a r e best fit by in t er n a l con version bet ween t h e t wo excit on st a t es of a st r on gly
cou pled bilin pa ir (F ig. 10). Th ey pr opose t h a t clu st erin g of ch r om oph or es wou ld pr ovide for m or e r a pid
m ovem en t of en er gy t o t h e lowest -en er gy ch r om oph or e fr om wh ich en er gy wou ld be t r a n sfer r ed ou t of
on e pr ot ein a n d in t o a n ot h er pigm en t . Also, F or st er
r eson a n ce t r a n sfer t o ot h er h igh er-en er gy ch r om oph or es wou ld be decr ea sed by ver y r a pid in t er n a l
con ver sion . Aft er t h e in t er n a l con ver sion , excit a t ion
wou ld loca lize on a pa r t icu la r bilin . Beck a n d Sa u er
(1992) a n d E din gt on et al. (1996) st u died t h e a lloph ycocya n in t r im er by a va r iet y of spect r oscopic m et h ods a n d con clu ded t h a t en er gy t r a n sfer wa s n ot
pr odu ced by F or st er r eson a n ce, bu t r a t h er r esu lt ed
fr om excit on st a t es pr odu ced by in t er a ct ion of t h e
bilin s a t a84 a n d b84. H om oelle et al. (1998) con t in u ed t h e st u dy of a lloph ycoca n in , u sin g a dva n ced
t ech n iqu es, a n d t im e con st a n t s of 56 a n d 220 fs wer e
a ssign ed t o r a dia t ion less deca y bet ween excit on

st a t es in t h e t r im er s. Th ese t r a n sit ion s wer e n ot

obser ved in pr epa r a t ion s of t h e a polypept ide fr om
C-ph ycocya n in . Ot h er t im e-r esolved flu or escen ce
st u dies h a ve a ppea r ed on t h e sepa r a t ed a a n d b
polypept ides of C-ph ycocya n in (F isch er et al., 1990),
a n d on t h e aB -con t a in in g t r im er (Ya m a za ki et al.,
1994).
Th e su m of t h ese st u dies su ggest s t h a t a ll t r a n sfer s on C-ph ycocya n in a n d a lloph ycocya n in m on om er s m a y occu r by F or st er r eson a n ce, a s well a s
som e of t h e t r a n sfer s on t r im er s, especia lly t h ose
in volvin g t h e b155 bilin of C-ph ycocya n in . Th e closely
spa ced a84/b84 pa ir on t r im er s of bot h bilipr ot ein s is
su bject t o fu r t h er in qu ir ies, bu t t h er e a r e sign ifica n t
r esu lt s for a lloph ycocya n in su ppor t in g deloca liza t ion . H igh ly soph ist ica t ed fem t osecon d la ser r esu lt s
(H om oelle et al., 1998) pr ovide com pellin g su ppor t
for excit on st a t es in t r im er s of a lloph ycoya n in . Deloca liza t ion bet ween pa ir s of bilin s h a s a lso been
su ggest ed for cr ypt om on a d bilipr ot ein s ba sed on
r esu lt s u sin g opt ica l spect r oscopy (Ma cColl et al.,
1995, 1998).
E a r lier t im e-r esolved en er gy t r a n sfer st u dies u sin g isola t ed bilipr ot ein s, bilipr ot ein com plexes, a n d
ph ycobilisom es h a ve been r eviewed (H olzwa r t h , 1986,
1991). Th ese cit a t ion s in clu de pion eer in g wor k don e
on bilipr ot ein s fr om r ed a lga e a n d cr ypt om on a ds, a s
well a s cya n oba ct er ia .
CYAN OB ACTERIA AN D HAB ITATS

P r eviou sly, it wa s n ot ed t h a t m a r in e cya n oba ct er ia

m igh t u t ilize t h e ligh t h a r vest in g pr oper t ies of Cph ycoer yt h r in a n d t h e CU-ph ycoer yt h r in s, a s well
a s com plem en t a r y ch r om a t ic a da pt a t ion in som e
ca ses, t o t h r ive in h a bit a t s of ch a n gin g a n d ch a llen gin g ligh t . Cya n oba ct er ia a lso live in su ch diver sit y a s
t h e pola r r egion s a n d t h er m a l h ot spr in gs. P h ycobilisom es h a ve been obser ved in a cya n oba ct er iu m ,
wh ich gr ows in h ot spr in gs a bove 70C (E dwa r ds a n d
Ga n t t , 1971). Ber n s, E dwa r ds, a n d co-wor ker s h a ve
sh own t h a t C-ph ycocya n in s pu r ified fr om t h er m oph iles h a ve differ en t wa ys t o m eet t h is ch a llen ge.
F or on e t h er m oph ilic cya n oba ct er iu m , t h e C-ph ycocya n in is t em per a t u r e r esist a n t a s fa ir ly la r ge
pieces of r od wer e st a ble fr om 10 t o 80C (E dwa r ds et
al., 1996, 1997). F or a n ot h er t h er m oph ile, t h e Cph ycocya n in is cold dissocia t ed a s t h e la r ger r od
pieces fa ll a pa r t a t low t em per a t u r e, bu t a r e a ssocia t ed n ea r gr owt h t em per a t u r es (Ber n s a n d Scot t ,
1966). Recen t ly, a t h er m oph ilic cya n oba ct er iu m wa s
lysed a n d yielded a C-ph ycocya n in a ggr ega t e of
t h r ee disks (H a ya sh i et al., 1997). Th is isola t e m a y
be t h e in t a ct r ods of t h e or ga n ism .
Th er e h a ve been t h er m odyn a m ic st u dies on t h ese
t h er m oph ilic C-ph ycocya n in s (Ch en et al., 1994).
Resu lt s a r e in t er pr et ed t o su ggest t h a t en t r opy

327

P H YCOBILISOME S

ch a n ges a r e qu it e sign ifica n t in t h e u n foldin g of

C-ph ycocya n in , a n d for t h er m oph ilic pr ot ein t h e
en t r opy con t r ibu t ion is even gr ea t er.
EP ILOGU E

Mu ch h a s been a ccom plish ed sin ce Ga n t t a n d

co-wor ker s bega n t o est a blish a st r u ct u r a l m odel for
ph ycobilisom es, wh ich so n icely pr odu ced u n derst a n din g of h ow t h ey wor k. Th e discover y of lin ker s
a n d t h e en su in g r esea r ch on bilipr ot ein s a n d lin ker s
pr odu ced lea ps of kn owledge wh ich m a de a com plex,
bu t en ligh t en in g st or y. St u dies on su ch a la r ge a n d
va r ia ble st r u ct u r e isola t ed fr om t h e diver se cya n oba ct er ia a n d t h e r ed a lga e a r e n ever r ea lly fin ish ed, bu t
wh a t a r e t h e key fea t u r es yet t o be est a blish ed?
On e issu e m a y st a n d ou t : t h e lin ker s h a ve been
n icely st u died, bu t wh a t is kn own a bou t t h e m olecu la r n a t u r e of t h eir in t er a ct ion wit h t h e bilipr ot ein s,
or h ow t h ey a ccom plish t h eir exqu isit e specificit y of
disk t o r od a ssocia t ion ? Next t o n ot h in g is t h e best
a n swer. Th er e a r e pu blish ed dr a win gs sh owin g t h e
lin ker occu pyin g t h e cen t r a l h ole in t h e bilipr ot ein
st r u ct u r e. Yes, it is clea r t h ey sh ou ld be t h er e, bu t is
t h er e pr oof? X-r a y cr yst a llogr a ph y st u dies h a ve been
ca r r ied ou t on b-ph ycoer yt h r in a n d B-ph ycoer yt h r in
fr om r ed a lga e (F icn er et al., 1992; F icn er a n d H u ber,
1993). Th e for m er la cked a lin ker a n d t h e la t t er
possessed on e. Th e lin ker st r u ct u r e wa s n ot obt a in ed
in t h ese st u dies, bu t t h e lin ker by com pa r ison of t h e
t wo bilipr ot ein st r u ct u r es is in t h e cen t r a l h ole of t h e
bilipr ot ein a n d does n ot pr ot r u de fr om it . Kessel et
al. (1973) h a ve pr odu ced elect r on m icr ogr a ph s of
C-ph ycocya n in disks fr om a cya n oba ct er iu m sh owin g a cen t r a l st r u ct u r e (F ig. 11). Th is object cou ld be
lin ker.
Som e qu est ion s: h ow do lin ker s in t er a ct wit h
bilipr ot ein s; sin ce t h ey do n ot pr ot r u de, h ow do t h ey
ca u se a specific bilipr ot ein disk t o a dd t o t h e r ods;
does on e lin ker in t er a ct wit h a n ot h er ; is t h er e a
con for m a t ion a l ch a n ge wh en lin ker join s disk or disk
join s r ods; wou ld lin ker fr om a t h er m oph ile con fer
t h er m ost a bilit y on m esoph ilic C-ph ycocya n in ; h ow
a r e t h e bilin s n ea r t h e cen t r a l h ole a ffect ed by
lin ker s; h ow does t h e L cm in n on h em idiscoida l ph ycobilisom es fu n ct ion ; does L cm in som e ver sion exist for
cr ypt om on a ds?
All of t h ese poin t s cou ld be t h e su bject of specu la -

F IG. 11. E lect r on m icr ogr a ph s of select ed views of ext r a ct s of

a cya n oba ct er ia l C-ph ycocya n in . Th ey sh ow disks wit h a cen t r a l
object .

t ion , bu t let u s t a ke on ju st on e. Th e b84 bilin s a r e

loca t ed ver y n ea r t h e cen t r a l ch a n n el in t h e disks.
Th e bilin s of C-ph ycocya n in a r e a ffect ed by lin ker s
a s in dica t ed by t h e effect s of lin ker s on t h eir spect r a
a n d en er gy t r a n sfer kin et ics. Th ese obser va t ion s
m a y su ggest t h a t bilin s a r e spa t ia lly displa ced by
lin ker s. If t h is is t r u e, wh a t is t h e st a t u s of ou r
u n der st a n din g of t h e r ou t es of en er gy m igr a t ion ?
Ch a n ges in bilin -t o-bilin dist a n ces a n d or ien t a t ion s
will sa lien t ly ch a n ge t h e ca lcu la t ion of h ow en er gy is
t r a n sfer r ed. It m a y be t h a t ca lcu la t ion s u sin g lin kerfr ee bilipr ot ein s a r e u sefu l bu t give a n in com plet e
view of t h e a ct u a l en er gy m igr a t ion syst em . Th e
open -ch a in st r u ct u r e of t h e t et r a pyr r oles m a y m a ke
t h em flexible in r espon din g t o ch a n ges t h a t r esu lt
fr om m odifica t ion of t h eir n ea r est n eigh bor en vir on m en t . Th e n a t u r e of lin ker s con t r ibu t es t o t h e difficu lt y in t h eir st u dy. A ph ycobilisom e con t a in in g fou r
disks, even if t h e disks a r e iden t ica l, will h a ve fou r
differ en t r od-r ela t ed lin ker s. Rem em ber lin ker s va r y
wit h ea ch disk m ovin g a m on g t h e r od, even if t h e
disks t h em selves a r e iden t ica l. A ph ycobilisom e disk
con t a in in g on e specific lin ker, in pa r t icu la r L RC ,
sh ou ld be st u died for r ea l pr ogr ess. An a logou sly,
exa m in in g t h e st r u ct u r e of a lloph ycocya n in wit h
lin ker a t t a ch ed wou ld be of in t er est .
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