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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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