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128
P r o k a r y o t e s a n d e u k a r y o t e s
s tr a t eg i es a n d s u c c e s s e s
Michael arlile
Rece nt developments in molecular biology and ecological theory ha ve illuminated the
evolutionary divergence betw een prokaryotes and eukaryotes. It is suggested that it is
inappropriate to regard the prokaryotes as primitive a nd the eukaryotes as advanced.
It is mo re fruitful to view the two groups as having adopted successful b ut alternative
evolutionary strategies in which proka ryotes h ave exploited the advantages of
miniaturization an d eukaryotes those o f size.
T h e a n a l y s i s o f r i b o s o m a P a n ti t R N A ~ is
beg inn ing to p rov ide molecu la r de ta i l tha t i s
revo lu t ion iz ing our unders tand ing of p ro-
karyote phylogeny and o f the relationships
betw een the ma jor groups o f cellular organ-
i s m s . A n e a r l y c o n s e q u e n c e o f t h is w o r k
has been the recog ni t ion of the a rchaebac-
te r ia as a g roup on ly d i s tan t ly re la ted to
o ther o rgan isms . This has l ed to c r i ti c i sm of
the d iv i s ion of ce l lu la r o rgan isms in to p ro-
karyotes a nd eukaryotes ~,* n fav our of class-
i f i ca tion in to th ree g roups , the a rchaebac-
Michael Carlile is at the Department of Pure and
Appl ied B iology Imperial C ol lege of Sc ience and
T e c hno logy L ondon SW 7 2B B U . K .
t e r ia , eubac te r ia (used in a se nse wider than
is usua l among bac te r io log is t s ) and
eukaryotes . I a rgue h ere tha t the d iv i s ion of
ce l lu la r o rgan isms in to p rokaryo tes and
eukaryotes remains a va l id one , re f lec t ing a
p r o f o u n d d i v e r g e n c e w i t h r e s p e c t t o
evolu t ionary s t ra teg ies and l i fe - s ty les . Th is
v iewp oin t is d i scussed e l sewh ere a t g rea te r
leng th .
Th e arehaebaeter ia a nd evo lut ionary
d i v e r g e n c e
The c lass o f a rchaebac te r ia cons i s t s o f
methane-genera t ing bac te r ia (methano-
gens) , a g roup of sa l t - to le ran t bac te r ia
(ha lophi les ) wi th a un ique photometabol -
T 1 B S - A p r i l 1 9 8 2
i sm and so me ac id- to le ran t the rmoph i les ,
They a re recog nised as a g roup on the bas i s
o f th e i r 1 6 S R N A c o m p o s i t i o n a n d s h a r e
some s t r ik ing b iochemica l fea tures which
are absen t f rom o ther bacter ia . I t seems
c l e a r t h a t t h e y m u s t h a v e d i v e r g e d f r o m
other o rgan isms ear ly in evo lu t ion : the
t h r e e p o s s i b l e p a t t e r n s o f d i v e r g e n c e o f
a rchaebac te r ia , eubac te r ia (used here and
subsequent ly in the b road sense) and
eukaryotes a re ind ica ted in F ig . 1 .
H o w e v e r , i n s p i te o f t h e e a r l y d i v e r g e n c e o f
the a rchaebac te r ia they resemb le o ther bac-
teria in their small s iz e and structural s impl-
ic i ty : these fea tures , a s wi l l be a rgued
b e l o w , a r e o f f u n d a m e n t a l e c o l o g i ca l a n d
evolu t ionary s ign i f icance and the produc ts
o f o n e o f t h e t w o m a j o r e v o l u t io n a r y t re n d s .
rokaryotes me tabol ic d ivers i ty and
m i n i a t u r i z a t i o n
A s tr ik ing fea ture o f p rokaryo tes i s the i r
m e t a b o l i c d i v e r s i t y . M o s t o f t h e
b i o c h e m i c a l p r o c e s s e s k n o w n i n
eukaryotes a l so occur in p rokaryo tes , bu t in
addi t ion there a re a wide var ie ty o f
ac t iv i t i es unknown in eukaryo tes , fo r
e x a m p l e a n o x y g e n i c p h o t o s y n t h e s i s ,
energy prod uc t ion by the ox ida t ion of inor -
g a n i c c o m p o u n d s ( c h e m o l i t h o t r o p h y ) ,
o x i d a t i v e m e t a b o l i s m b a s e d o n e l e c t r o n
- % - 2 - - _ - -
: - - J . . o . . . o J
-- ~ ~ . . . . . . . . / W E C N < T
OUT-RUt4. ~
~ ~. ,TPI ESP MUL f iCELL
O R G A N I S fV U ; ]
~) Elsevier Biomedical Press 1982 0376 - 5067/82/0000 - 0000/ 02.75
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T I B S - A p r i l 1 9 8 2
a c c e p t o r s o t h e r t h a n o x y g e n ( n i t r a t e , s u l -
p h a t e a n d c a r b o n d i o x i d e ) , a w i d e v a r i e t y
o f p a t h w a y s f o r p y r u v a t e f e r m e n t a t i o n ,
m e t h a n e p r o d u c t i o n a n d u s e a n d n i t r o g e n
f ixa t ion . I t i s c lea r tha t p rokaryo tes cou ld
m a i n t a i n a b i o s p h e r e : a n y e s s e n t i a l e l e m e n t
t h a t i s o x i d i s e d b y s o m e p r o k a r y o t e s c a n b e
r e d u c e d b y o t h e r s .
M a n y p r o k a r y o t e s h a v e h i g h m e t a b o l i c
r a t e s, g r o w f a s t a n d h a v e s h o r t g e n e r a t i o n
t i m e s - a b o u t 2 0 m i n i n E s c h e r i c h i a c o l i .
T h i s e n a b l e s t h e m t o b e h i g h l y c o m p e t i t i v e
u s i n g n u t r i e n t s t h a t a r e o n l y a v a i l a b l e f o r a
s h o r t p e r i o d o f t i m e . T h e y a r e a l s o m o s t l y
s m a l l - E . c o i l h a s a v o l u m e o f a b o u t 1 / . tm3
w h i c h m e a n s t h a t a l a r g e p o p u l a t io n c a n
b e p r o d u c e d o n l i m i t e d n u t r i e n t s . L a r g e
n u m b e r s r e d u c e t h e c h a n c e o f r a n d o m
e x t i n c t i o n , s o p r o k a r y o t e s a r e a b l e t o e x -
ploit resources that are too limited to support
a p o p u l a t i o n o f l a rg e r o r g a n i s m s . T h e s m a l l
s i z e a n d h i g h m e t a b o l i c a c t i v i t y o f
p r o k a r y o t e s m e a n s t h a t t h e i r n u m b e r s a n d
t h e i r c o n t ri b u t i o n t o t h e f l o w o f e n e r g y ,
c a r b o n a n d n i t r o g e n i n t h e b i o s p h e r e i s h i g h
in re la t ion to the i r b ioma ss .
Archaebacteria
a ~ Eubacteria
Prokaryotes
Eukaryotes
b ~ Eubacteria
Archaebacteria
Eukarkyotes
Prokaryotes
c
Eubacteria
Archaebacteria
Eukaryotes
Prokaryotes
4 3 2 1 0
PAST PRESENT
Approximate ime
in m illionsof
years
Fig. 1 . Three poss ib le patte rns for the d ivergence o f th e archaebac ter ial , eubac ter ia l and eukary ote l ines
fro m a co mm on ances tor ab out 40 00 mi l l ion yea rs ago. Sche me (a) represents a very ear ly divergence o f the
e u k a r y o t e l i ne ; ( b ) e m e r g e n c e o f e u k a r y o t e s f r o m t h e e u b ac te r ia s a n d ; ( c ) e m e r g e n c e o f e u k a r y o t e s f r o m
the archaebacteria ~2.~3. Al l three schem es a l low for the dev e lopm ent o f the charac ter ist ic eukar yote features
( represented - - - )occ urr ing during the sam e per iod, an d for the prokary ote -eu kar yot e d ivergence be ing
the mos t s ignif icant and pers istent o f evolut io nary trends .
129
E u k a r y o t e s s i z e a n d c o m p l e x i t y
E u k a r y o t i c m i c r o o r g a n i s m s a n d c e l l s
v a r y g r e a t l y i n s i z e b u t a r e u s u a l l y m u c h
l a r g e r t h a n t h o s e o f p r o k a r y o t e s . L i n e a r
d i m e n s i o n s t e n t i m e s t h o s e o f p r o k a r y o t e s
( e .g . 1 0 / x m i n s te a d o f 1 / x m ) a n d h e n c e
v o l u m e s a t h o u s a n d f o l d g r e a t e r t h a n p r o -
k a r y o t e s ( e . g . 1 0 0 0 / x m : ' i n s t e a d o f I / x m ~)
a r e c o m m o n . T h e r e s u l t i n g l o w e r s u r f a c e /
v o l u m e r a t i o s r e d u c e t h e r a t e s a t w h i c h
m e t a b o l i t e s c a n b e e x c h a n g e d w i t h t h e
e n v i r o n m e n t , a l t h o u g h c y t o p l a s m i c s t re a m -
i n g , c o n f i n e d t o e u k a r y o t e s , p a r t l y o v e r -
c o m e s t h e l i m i t a t i o n s o f d i f f u s io n . N e v e r -
t h e l e s s , m e t a b o l i c r a t e s a n d h e n c e g r o w t h
r a t e s a n d r e p r o d u c t iv e r a t e s a r e m u c h l o w e r
t h a n i n p r o k a r y o te s - g e n e r a t i o n t i m e s a s
s h o r t a s l h a r e k n o w n o n l y i n a f e w
e u k a r y o t e s . T h e l o w g r o w t h r a t e o f
e u k a r y o t e s m e a n s th a t t h e y c a n n o t c o m p e t e
w i t h p r o k a r y o t e s i n t h e s c r a m b l e f o r r e a d i ly
u s a b l e n u t r i e n t s a n d t h e i r l a r g e s i z e m e a n s
t h a t v i a b l e p o p u l a t i o n s c a n n o t b e b u i l t u p s o
eas i ly .
A l t h o u g h t h e m e t a b o l i c a c t i v i t i e s o f
e u k a r y o t e s a r e l e s s d i v e r s e t h a n t h o s e o f
p r o k a r y o t e s , e u k a r y o t e s d o h a v e m a n y f e a -
tu res tha t p rokaryo tes lack - the re a re 22
s u c h f e a t u r e s u n i v e r s a l l y p r e s e n t a n d n i n e
m o r e t h a t a r e c o m m o n i n e u k a r y o t e s L
M a n y s u c h f e a t u r e s c o n c e r n u l t r a s t ru c t u r a l
o r g a n i z a t i o n w h i c h i s m u c h m o r e c o m p l e x
t h a n i n p r o k a r y o t e s . T h e p r e s e n c e o f a c t in
m i c r o f i l a m e n t s a n d t u b u l i n m i c r o t u b u l e s
a r e o f p a r t i c u l a r s i g n i f i c a n c e , b o t h i n p a r -
t i a l l y o v e r c o m i n g t h e l i m i t a t i o n s i m p o s e d
o n s i z e b y d i f f u s i o n r a te s , a n d i n b r i n g i n g
a b o u t t h e c e l l s h a p e c h a n g e s i n v o l v e d i n
e n g u l f i n g s o l i d p a r t i c l es ( p h a g o c y t o s i s ) .
T h i s a b i l i ty m a k e s i t p o s s i b l e f o r e u k a r y o t e s
t o e x p l o i t p r o k a r y o t e s , e i t h e r b y p r e y i n g o n
t h e m a n d t h u s o b t a i n i n g a b a l a n c e d d i e t
w i t h m i n i m a l b i o s y n t h e t i c e x p e n d i t u r e o r
b y h a r b o u r i n g t h e m a s e n d o s y m b i o n t s a n d
u s i n g t h e i r b i o c h e m i c a l v e r s a t i l i ty . C h l o r o -
p l a s t s a l m o s t c e r t a i n l y o r i g i n a t e d a s
e n d o s y m b i o n t s a n d m i t o c h o n d r i a m a y h a v e
d o n e s & - 5. T h u s e u k a r y o t e s d e p e n d o n
p r o k a r y o t e m e t a b o l i s m f o r t h e i r a b i l i ty t o
u s e s o l a r e n e r g y a n d p e r h a p s t o p e r f o r m
o x i d a t i v e p h o s p h o r y l a t i o n .
E u k a r y o t e s h a v e c o m e t o d o m i n a t e
a e r o b ic e c o s y s t e m s a s p r i m a r y p r o d u c e r s
a n d i n t e r m s o f b i o m a s s , s p e c ie s n u m b e r s
a n d m o r p h o l o g i c a l d i v e r s i t y . L a r g e s i z e h a s
p e r m i t t e d a n i m a l s t o h a v e a r a t e o f m o v e -
m e n t , d e g r e e o f i n d e p e n d e n c e o f t h e e n v i -
r o n m e n t a n d s o p h i s t i c a t e d s e n s o r y a n d
m o t o r s y s t e m s i m p o s s i b l e i n p r o k a r y o t e s .
r s e l e c t i o n a n d t h e e v o l u t i o n o f
p r o k a r y o t e s
T h e c o n c e p t o r r - a n d K - s e l e c ti o n , w h i c h
h a s p r o v e d f r u i t f u l i n a n i m a l a n d p l a n t
e v o l u t i o n a r y e c o l o g y 8 , has recen t ly been
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1 3 0
a p p l i e d t o t h e e v o l u t i o n a r y d i v e r g e n c e o f
p r o k a r y o t e s a n d e u k a r y o t e s 4 an d f o r m u -
l a t e d m o r e r i g o u r o u s l y t h a n h i t h e r t o 7 . T h e
s y m b o l s a re f r o m a n e q u a t i o n o f p o p u l a t i o n
g r o w t h ; r r e p r e s e n t s t h e i n t r i n s i c r a t e o f
i n c r e a se a n d K t h e c a r r y i n g c a p a c i t y o f t h e
e n v i r o n m e n t , r - s e l e c t i o n w i l l o p e r a t e
w h e r e t h e r e a r e d r a s t i c f l u c t u a t i o n s i n a v a i l -
a b l e n u t r i e n t s ; d u r i n g p e r i o d s o f a b u n -
d a n c e , e x p l o s i v e g r o w t h w i l l o c c u r a n d v a r i -
a n t s w i t h t h e h i g h e s t g r o w t h r a t e w i l l l e a v e
m o s t p r o g e n y . K - s e l e c t i o n o p e r a t e s w h e r e
a r e s o u r c e i s c o n s t a n t l y a v a i l a b l e b u t i n
l i m i t e d a m o u n t s ; h e r e o r g a n i s m s w i l l ra r e l y
b e a b l e t o a c h i e v e h i g h g r o w t h r a t e s a n d t h e
a b i l i t y t o s u r v i v e a h a r s h e n v i r o n m e n t , i n -
c l u d i n g c o m p e t i t o r s a n d p r e d a t o r s , w i l l b e o f
g r e a t e r i m p o r t a n c e i n l e a v i n g p r o g e n y .
S p l i t g e n e s a n d R N A s p l i c i n g ar e c o m -
m o n i n e u k a r y o t e s 8 b u t h a v e n o t b e e n
d e t e c t e d i n p r o k a r y o t e s . I t h a s b e e n s u g g e s -
t e d ~ .~ ° t h a t i n t h e e a r l i e s t o r g a n i s m s t h e
f i d e l it y o f D N A d u p l i c a t i o n a n d t r a n s c r i p t-
i o n w o u l d h a v e b e e n l o w a n d i n t r o n s a n d
R N A s p l i c in g w o u l d h a v e h a d a n i m p o r t a n t
r o l e . C e l l s c o u l d w e l l h a v e b e e n l a r g e b y
t h e s t a n d a r d s o f p r e s e n t d a y p r o k a r y o t e s
a n d h a v e h a d m u l t i p l e c o p i e s o f D N A . T h e
i n t e n s i v e l y s t u d i e d p r o k a r y o t e s , s u c h a s E .
coli, h a v e l i tt l e n o n - c o d i n g D N A ; m o s t o f
t h e i r g e n e s a r e o n a s i n g l e c i r c u l a r c h r o m o -
s o m e a n d g e n e s c o n c e r n e d w i t h r e la t e d
f u n c t i o n s a r e c l u s t e r e d a n d c o - o r d i n a t e l y
r e g u l a t e d a s o p e r o n s . T h e s e m a y w e l l b e
h i g h l y a d v a n c e d f o r m s , s u p r e m e
r - s t r a t e g i s t s a n d m a r v e l s o f m i n i a t u r i z a t -
ion .
S o m e o f t h e l a r g e s t p r o k a r y o t e s a r e t h e
p h o t o t r o p h s a n d s o m e c h e m o l i t h o t r o p h s ,
w h i c h e x p l o i t l i m i t e d b u t p e r s i s t i n g
r e s o u r c es . S o m e o f t h e s e o r g a n i s m s h a v e
h i g h D N A c o n t en t s c o m p a r e d w i t h E. coli
( T a b l e I ) a n d m a y p r o v e t o h a v e s u c h f e a-
t u r e s a s i n t r o n s . I n d e e d , i t i s p o s s i b l e - i f
t h e s y m b i o t i c t h e o r y o f t h e o r i g i n o f
c h l o r o pl a s ts a n d m i t o c h o n d r ia i s a c c e p t e d -
t h a t in t r o n s h a v e a l r e a d y b e e n d i s c o v e r e d i n
t h e s e l a rg e p r o k a r y o t e s w h i c h d o n o t n e e d a
h i g h r e p r o d u c t i v e r a te .
K selection and eukaryote evolution
A s i n d i c a t e d a b o v e , t h e r e a r e a t l e a s t 2 2
f e a t u r es u n i v e r s a l l y p r e s e n t i n e u k a r y o t e s
a n d a b s e n t i n p r o k a r y o t e s . S o m e o f t h e s e
m a n y p r i m i t i v e f e a t u r e s w h i c h h a v e s u r -
v i v e d f r o m t h e e a r l i e s t c e l l s , b u t o t h e r s a r e
b i o c h e m i c a l l y o r s t r u c t u r a l l y c o m p l e x a n d
m u s t h a v e b e e n a c q u i r e d m o r e r e c e n t l y .
M o l e c u l a r d e t a i P 2 s u g g e s t s a n e a r l y
d i v e r g e n c e f r o m s u r v i v i n g p r o k a r y o t e
l i n e s , y e t e u k a r y o t e s d i d n o t m a k e a n y s t ri k -
i n g c o n t r i b u t i o n t o t h e f o s s i l r e c o r d u n t i l
a b o u t 1 0 0 0 m i l l i o n y e a r s ag o . I t s e e m s
l i k e l y , t h e r ef o r e , t h a t f o r a v e r y l o n g p e r i o d
TAB LE 1.
ApproximateDNA content and tx~tential odingcapacityof variousorganisms
TIBS - Apri l 1 982
Organism DNA content
(base pairs × 10~)
Coding capacity
(numbers of
different
polypetidesof
307 amino acids)
Prokaryotes
Small mycoplasma 1.6 1600
Escherichia coli 4 4000
Large cyanobacterium 16 1600(I
Eakaryoteorganelle
Bakers yeast mitochondrion 2-3 2000-3000
Eukaryotes
Sm all yeast species 5 50(~)
Bakers yeast 12 20 12000-20000
Range in mamm alian pecies 2800-5300 2.8-5.3 × 10~
Range in protozoa 55-32000(I 55 × 10~-320 × 10~
Data based on Table 4 in R ef. 4 and sources here cited
t h e e u k a r y o t i c l i n e w a s r a t h e r u n s u c c e s s f u l ,
b u t t h a t at a c e r ta i n p o i n t - w h e n
e n d o c y t o s i s p e r m i t t e d p r e d a t i o n a n d
e n d o s y m b i o s i s - t h e y b e c a m e o u t s ta n d -
i n g l y s u c c e s s f u l a n d d i v e r s i f i ed . T h e r e a r e
o t h e r e x a m p l e s o f l o n g o b s c u r e g r o u p s
e v o l v i n g f e a t u r e s t h a t u l t i m a t e l y l e d t o o u t s -
t a n d i n g s u c c e s s . T h e m a m m a l s a re o n e
s u c h e x a m p l e , a n d w i t h i n t h e m a m m a l s ,
t h e l i n e t h a t l e d t o m a n .
M a j o r e u k a r y o t i c a c t i v i t i e s a r e t h e u s e o f
l i g h t e n e r g y ( p l a n t s a n d p h o t o s y n t h e t i c
m i c r o o r g a n i s m s ) a n d p r e d a t i o n ( a n i m a l s
i n c l u d i n g p r o t o z o a ) . I n b o t h i n s t a n c e s , v i o -
l e n t f l u c t u a t i o n i n t h e a v a i l a b i l i t y o f
r e s o u r c e s i s l e s s l i k e l y t h a n i t i s f o r m o s t
p r o k a r y o t e s s o K - s e l e c t i o n is e x p e c t e d t o
b e m o r e i m p o r t a n t i n t h e e v o l u t i o n o f
e u k a r y o t e s . S i z e i n c r e a s e s i n p r i m i t i v e
e u k a r y o t e s w o u l d h a v e e n h a n c e d t h e i r a b il -
i t y to p r e y o n s m a l l e r c e l l s , a n d t o h a r b o u r
e n d o s y m b i o n t s . M a x i m u m s p e e d in a bs o -
l u t e t e r m s ( e . g . i n / z m s t ) is p r o p o r t i o n a l
t o s i z e , s o l a r g e r c e l l s c a n m o v e g r e a t e r d i s-
t a n c e s i n se a r c h o f p re y . H o w e v e r , t h e i r
s p e e d i n t e r m s o f b o d y - l e n g t h s / s 1 i s l es s ,
a n d t h i s , t o g e t h e r w i t h l a r g e s i z e , m a k e s
s p a t i a l s e n s i n g f e a s i b l e , a s i t i s e a s i e r t o d i s -
c r i m i n a t e b e t w e e n s t i m u l i a t d i f f e r e n t
p o i n t s o n t h e b o d y s u r f a ce . S p a t i a l s e n s i n g
m a y h a v e m a d e c o - o p e r a t i o n b e t w e e n c e l l s
t o f o r m m u l t i c e l l u l a r o r g a n i s m s , a n d t h e
d e v e l o p m e n t o f v a r i o u s fo r m s o f s y m b i o s i s ,
e a s i e r .
A s t r i k i n g fe a t u r e o f e u k a r y o t e s , c o n -
t r a s ti n g w i t h p r o k a r y o t e s , i s t h e r a n g e i n t h e
h a p l o i d D N A c o n t e n t o f t h e ir n u c l e i ( T a b l e
I ) . I t i s c l e a r f r o m t h e e x a m p l e o f y e a s t s t h a t
t h e c o d i n g r e q u i r e m e n t o f s o m e e u k a r y o t i c
m i c r o o r g a n i s m s i s l i t tl e g r e a t er t h a n t h a t f o r
E. coli. H o w e v e r , s o m e e u k a r y o t e s c o nt a i n
D N A f a r i n ex c e s s o f a n y c o n c e i v a b l e c o d-
i n g r eq u i r e m e n t , i n d i c a t i n g t h a t m u c h o f
t h e D N A h a s o t h e r r o l es . L a r g e c e l l s t e n d t o
h a v e l a r g e n u c l e i , a n d i n th e p r o t o z o a t h e
g r e a t r an g e i n D N A c o n t e n t t e n d s t o r e fl e c t
c e l l si z e , s u g g e s t i n g t h a t m u c h o f t h e D N A
h a s a n u c l e o s k e l e t a l r o l e . I t i s s u g g e s t e d
t h a t in e u k a r y o t e s , i n t r o n s w e r e p r e s e r v e d
a n d p e r h a p s u s e d r a t h e r t h a n e l i m i n a t e d .
F i l a m e n t o u s f u n g i an d y e a s t s , h o w e v e r ,
h a v e o s m o t r o p h i c ( n u t r i e n t a b s o r b i n g )
r a t h e r t h a n p h a g o t r o p h i c n u t r i t i o n a n d i n
t h i s r e s e m b l e m a n y b a c t e r i a , w i t h w h i c h
t h e y a r e i n c o m p e t i t i o n . I n t h e s e l i n e s t h e
g e n o m e i s l it t l e l a r g e r t h a n i n p r o k a r y o t e s ,
t h e re i s l i t t l e r e p e t i t i v e D N A a n d i t i s l i k e l y
t h a t , a s in m o s t p r o k a r y o t e s , m o s t n o n -
c o d i n g D N A h a s l a r g e ly b e e n e l im i n a t e d b y
r - s e l e c t i o n .
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