Comparisons of complete 16S ribosomal ribonucleic acid (rRNA) sequences established that the secondary structure of these molecules is highly conserved. Earlier work with 5S rRNA secondary structure revealed that when structural conservation exists the alignment of sequences is straightforward. The constancy of structure implies minimal functional change. Under these conditions a uniform evolutionary rate can be expected so that conditions are favorable for phylogenetic tree construction

Fox, G. E.

English

NASA Technical Reports Server

N8 5 - 32 7 19 
Comparisons of complete 16s ribl;somal r ibonuc le ic  acid 
( rRNA)  sequence% have establ  i shed t h a t  the  secondary s t ruc tu re  of 
these molecules is. h igh l y  conserved. E a r l i e r  work w i th  5s rRN6 
secondary s t ruc tu re  revealed tha t  when s t r u c t u r a l  conservation 
e x i s t s  the  alignment of sequences is straightforward. 
Furthermore the  constancy o f  s t ruc tu re  imp1 i e s  m i n i m a l  funct ional  
change. Under there condi t ions a reasonably uniform evolut ionary 
r a t e  can be? expected so t h a t  condi t ions are favorable f o r  
ph y l  ogenet i c t r eet conset ruc t i on. 
The sequences o f  a l l  t he  16s ribosomal RNA ol igonucleot ide6 
produced by complete d igest ion w i t h  r ibonuclease T1  al lows 
the  const ruct ion of rRNCI "catalogs" fr-am a la rge  va r ie t y  of 
organisms. Binary comparisons of  these catalogs are Gsed t o  
generate a matr ix o f  associat ion c o e f f i c i e n t s  (Sam values) 
from which dendrograms, thought t o  be p a r t i a l  phylogenies, can be 
c o n s t r ~ t e d .  Complete 5s rHN4 sequences e x i s t  f o r  many o f  the  
same organisms such t h a t  separate dendrograms can be made from 5s 
rRNA data. 
The major f i nd ing  of these stcidies i s  t h a t  three 
we1 1-separated evolut ionary l i n e s  of descent can be detected 
which are a t  present represented by eukaryotes, archaebacteria, 
and eubacteria (Fig. 1-71. Presumably, a l l  three l i n e s  of 
descent have diverged from the  same ancestral bac te r ia l  
populations. T h i  s branching may have occurred, however , bef or-e 
the  evolut ion o f  the  genetic apparatus w a 5  complete. These three 
l ineages d i f f e r  i n  morphology of the  small ribosomal subunit a5 
wel l  (Fig. 1-81. 
Within the  two prokaryot ic  l i n e s  of  descent a t  l eas t  twelve 
major groups are detected; two archaebactcri a1 and ten  
eubacterial.  F i ve  o f  the  eubacter ia l  groups contain 
photosynthetic organisms so tha t  it i s  apparent t h a t  the various 
types of photosynthesis are po lyphylet ic  (Fig. 1-3). Only seven 
species of  cyanobacteria are represented bu t  even so i t  i s  c lear  
tha t  th is  cyanobacterial l ineage includes both Prochloron and 
the rhodoplast of  P o r p h y r i d i u m .  The p lan t  and €wglena 
chloroplasts  share a common ancestry w i t h  those seven 
cyanobacteria as they are cu r -en t l y  represented on these trees. 
Together then the  cyanobacteria and ch loroplasts  def ine a s ing le  
major group of  photosynthetic eubacteria. The photosynthetic 
f 1 ex  i bacter i u m  Chl or0 f l  e x u s  surantiacus and the Chl orobi aceae 
apparently represent unrelated groups. The recent ly  discovered 
Heliothrix belongs t o  the  Gram p o s i t i v e  bac ter ia  and f o r  the 
f i r s t  t ime br ings  photosynthesis t o  tha t  order-. The nonsulfur 
https://ntrs.nasa.gov/search.jsp?R=19850024406 2020-03-20T18:20:22+00:00Z
purple photosynthetic bacteria cluster exclusively into the, fifth 
group with many non-photosynthetic respiring bacteria (Fig. 
I - 1 0 )  . 
The three best-characterized branches of the purple bacteria 
are referred to as the alpha, beta, and armma subgroups. The 
majority of the Rhodospirillaceae contain lamellar or vesicular 
intercytoplasmic membranes and are in the alpha subgroup where 
they can be further subdivided according to criteria such as 
helical form, asymmetric cell division, and the presence of a 
split 23s rRNA. Each of the subgroups contains 
non-photosynthetic genera, suggesting that photosynthesis has 
been gei ned and/or 1 ost several ti mer dur i ng bactsr i a1 eval uti on. 
The Rhodorpirillaceae with tubular intracytoplasmic membranes are 
simi larly interspersed among non-photosynthetic organisms in thE 
"beta" subgroup (Fig. 1-10]. The Chromatiaceae, including 
members of the genera Chroartiur, ' ih iocapsr ,  and 
Lctothzorhodospira ere local ired in the "gamma" subgroup. 
The purple group is of special interest because several of 
its members have been Fuggested as being involved in 
endosymbiotic relationships which ultimately gave rise to 
eukaryotic mitochondria. 5s rRNA sequence has already given 
strong support for the origin of plant mitochondria from the 
alpha subgroup. Mitochondria are, however, probably of 
polyphyletic origin, as they can be readily divided between those 
with tubular cristae and those with flattened (lamellar or 
vesicular) cristae. Since the alpha and beta subgroups of the 
purple bacteria can be distinguished by the same criteria, it 
seems likely that each subgroup may have separately given rise to 
some eukaryotic mitochondria. In the +u:ure it may be possible 
to localize mitochondrial origins in these two subgroups with 
even greater precision. 
Bonm,  L., Doolittlr, W.F. and Fox,  &E., 1979. 
Cyanobacterial evolution: Results of 16s ribosomal 
ribonucleic acid sequence analysis, Can. J. biorhem., 
57: 879-888. 
Fox, &E., Luhrsen, K.R. and Woeso, C.R., 1982. 
Archaebacterial 5s ribosomal 3NA, Zbl. Bakt. :lyg. I Abt. 
Orig C, m:330-345. 
Fox, &E., Pechrm, K.R. and be-, C-R., 1977. Comparative 
cataloging of 16s ribosomal RNA - A molecular i proach to 
prokaryotic systematics, Int. J. Syst. Bacteriol., a: 44-57. 
31 
Fox ,  @.E., Gtackebrrndt, E., Hespell ,  R.B., Oibeon, J . ,  
Hani lof f ,  J . ,  Dyer, T.A. ,  Wolfe, R . S . ,  Balch, W.E., Tanner, 
R.S., Magrum, L . J . ,  Zablm, L.B. ,  B l a k e m o r a ,  R . ,  Gupta, R., 
h e n ,  Lo,  Lawir, B . J . ,  Stahl, D.A., Lulchrsen, K.R., Chen, 
K.N. end Womsa, C.R., 1480. The phylogeny OC prokarvotes, 
Science, z)C: 457-463. 
Seewaldt, E. and Stackebrandt, E. 1982. Partial sf :r':ence of 
16s r!.borsomal RNA and the phylogeny 05 Prochloron,  
Nature, 225: 618-620. 
Sobierki ,  J., Chm, K.N., Fi l i ea treau ,  3. , Picket t ,  M.H. end 
Fox,  1984. 16s r R N A  oligowcleotide catalog data 
base, Nucleic Acid R e s . ,  1.2: 141-148. 
Stackebrandt, E. and Woese, C.R., 1981. The evolution of 
prokarvotes. In Molecular and C e l l u l a r  Aspects  o f  
Nicrohial  €vo luK. ion .  (M.J. Carlile, J.F. Collins and 
B.E. b. Moseley, eds. 1 ,  32nd SOC. Gen. Mi .-r-oaiol. Symposium. 
52: 1-32. 
Stackebrandt, E., Ludwig, W., and Fox ,  G.E., 19815. IbS 
ribosomal RNA oligonucleatide cataloging, Mekhods in 
Microbiol. , 12. (in press). 
Stewart, K.D. and t lat tox ,  K.R.. 1984. The case for a 
polyphyletic origin 06 mitochondria: morphological and 
molecular comparisors. J. Mol. Evol . .  2l-354-57. 
Villanueva, E., Luehr8en, K . R . ,  G k b o n ,  J. :  Del ihas,  N., and 
Fox ,  G.E., 1985. Localization and the phylogenetic wiqin 
05 the plant mitwhondrion based on a cornparativy anal/Ciis 
of 5s ribosomal RNA sequences, J. Mol. Evol, (in press). 
Woese, C.R.,  Gibson, J . ,  and Fox,  G. E., 19SO. 00 
genealogical patterns in purple photosynt-hetic bacteria 
reflect interspecific c,.me transfer'? p i , .  Cure. 
2@:212-214. 
Woese, C.R. ,  Stackebrandt, E., Weisburq, W.G., Pasteur, B . J . ,  
Madigan, M.T., Fowler, V.J., Hahn, C.M., Dlanz, P., Gupta, 
R., Neelson, K.H. and Fox,  G.E.. 1984. lhe phvloqeny of 
purple bacteria: The alpha subdivision, Syst. Appl. 
Microbiol.. 3; 315-326. 
32 
OMGtNAL: P F S  '& 
OS POOR QUALITY 
Subunits Type of Nud2a of 8i2e of 
rolecules roiecU1.S wbwrita 
166 rRW 1 
protei ne 22 
2900 mKte0tid-S 
120 mrcl+otid+r . i f f a r . t  proteins 
(L1 -Lu) 
Figure 1-7. Caaparison of ribosomal macronolecules. Five S 
riboscrnal FillF~ sequences showing structures of ( l e f t >  d 
nematadc !C. ~ I e g a n s )  and E .  c o l i ,  d eubacterium. 
summarv of L i e  structure and macromolecular compos1 t 1 on 
of t)acterr,tI riboscmes is Shawn at the bottom. { R i g h t )  F i v e  
S R ? M  f r o m  five "archaebacteria." N o t e  the 108 rwrleutide 
inser t : i . -$  in H ~ ~ C ~ C O C C U S .  nearly tne s i r e  of the . -st af 
the 5s !.!$ ..lolecLlie. 
33 
34 
Table 1-4. 
ARCHkbEBACTER 1 #3 
De+ining Criteria 0 .  kchaebrcterial Prokuyotm 
-a -. - 
1. Major l i p i d s  are ether l i nked  w i t h  p5ytan31 s ide  
c h a i i s  (Cno). I n  other bac ter ia  and 
eukarbotes major l i p i d s  are ester l inked. 
2. Eased on 16s ribosomal RNA o l igonucleot ide 
catalogues these organisms are more c lose l \ ,  
r e l a t e d  t o  each other t h a n  they are t o  
eukaryotic or  other bac te r ia l  16s RNGis. (169 
rRNA from s m a l l  ribc:somal subunits is about 1540 
nucleot ides long). 
3. Eased on the sequence of nucleot ides i n  5s  
ribosomal RNA these organisms are more c lose ly  
re la ted  to each other than thev are to 
eukaryotic or  other bac te r ia l  5s RNAs. (55 rRNA 
from la rge  ribosomal subunit i s  about 120 
nucleot ides long, Fig. 1-7). 
4. Archaebacteria lack: peptidoglycan i n  t h e i r  c e l l  
walls. 
5. CI s ing le  DNb dependent-RNA polymerase w i t h  complex 
subunit s t ruc tu re  (more than 6 subunits) i s  
present i n  arctjaebacteria. 
6. Archaebacteria ribosomes have a d i s t i n c t i v e  shape. 
iFiq. 1-8). (Lake. 1983.) 
7. Archaebacteria include: 
A l l  methanoqenic bac ter ia  
Hal ophi 1 i c and thermoaci dophi 1 i c hacter i a: 
Si l l  fo l  O b u J  H a l  O C O C C ~  
T b e r ~  proteus N a I  obacteriur 
Des& f <c~~coccus T h e r w o p l  aswa acidophi l  
35 
Table 14.  
continued 
, .__- .- 
Ranges ot ELt, values: 16s ribosomal RNA 
The lower l i m i t  of the range of  Sab values from 
01 iqonucleotide catalogues amonqst t h e  
archaebacteria are (3.18 t o  0.24. amongst the  
eubacter-ia C.17 - 0.22. The data f o r  the 
ch loroplasts  (0.28 - 0.32 w i t h  cvanobacteria) 
and t-hodoplasts (0.40 - 0.43 w i t h  cvanobacteria) 
ar-e included. The Sab values between the 
archL<ebacteria and eubacteria are between i r . O o  
t o  0.1q between the  eukaryotes and 
archaebacteria O . i i 7 - C ) .  10, and between the 
eukaryotes and eubacter i a 0. OS - CI. l i b .  
Cataloaues are avai lab le for- about 4 G G  aener a. 
RIBOeOME MORPHOLOQV F i g u r e  1-8. 
Fox, 6.E.. 1981. Arcliaebacteria, ribosomes arrd 
or- io in of  eucaryotic c e l l s .  I n  E s , o l d t . z o n  Tou'av.  
(Scudder and Seveal . eds. i . Univ. Mary1 and f:'ress. 
Ct.11 I eqe F a r  1.. , ME. pp. 235-244. 
P r o c .  2nd I n t n .  cony. o f  L ; v _ - - t .  and E v o l  . Szol . . 
L a k e ,  J.A.. 1493. Ribosome evolut ion --. the 
s t ruc tu ra l  basis fo r  p ro te in  synthesis i n  
archsebacteria. eubacceria and eukar yo+e%. Cell. 
3s: Tia-zi'?. 
Uoese, C.R. and Fox, 6.E.. 1'771. Phvloqanetic 
s t ruc tu re  of  the prokaryot ic domain: The primar',' 
I inodcirns. Proc. Natl .  ficad. Sciences. USH. 
7 3 : 5 C w 3  -5i)9(>. 
Comparative 
morphology OF 
the 30s ribosomal 
subuni t . 
Woe-, C.R., Hagrum, L.J. and Fox,  6.E.. 137U. 
ihrchaebacteria. J. Molec. E v o l . .  11:245-'5'? - -. 
36 
I I 
0 2  0 3  OQ O S  06 0 7  0 0  09 1.0 
8rO 6 .  Fox  
Figure 1-9. Partial phylogenies b a d  on 16s RNCI comparative data 
suggest that photosynthesis evolved separataly i n  different 
bacterial lineages. Xt probably evolved at l east  thrce t . i m a s  
(Green photosynthetic uacteria, e.q., Chlorohluo,  ( I e S t i .  
p u r p l e  photosynthe ic bacteria ( left  and riqht) and 
c ~ a n o b a c t c r i a / p l a s t i d ~  (left and right). The+ relationship 
between certa in  respirinq and their presumro ohotosynthetsr 
relatives is shown i n  more detail a t  right. 
38 
Figure 1-10. Based on 1& RNCI oligonucleatide catalogues there 
are at least three groups of photosynthctic/respiring 
bactwia,  One 04 w h i c h  iRhodomicrobiua. Paracoccus 
and many Rhodopseudoranas species. those w i t h  flattened 
membranes) is shown in detail h e r e .  Another presumed lincaqc, 
the beta group (lower right). has tubular membranes. 
Mitochondria of eukaryotes  are thought to d e r i v e  from these 
barterial lineages. Most likely t h e y  too ar-e polyphyletic, 
those with f la t tened cristar (e .q .  animals and p1a:Jt.j) c o m i n q  
f r o m  t h e  alpha group and those w i t h  tubular cristae te.q., 
ciliates, chrysophvtes )  f r o m  t h e  b e t a  uroup. 
39 


Insights into the phylogenetic positions of photosynthetic bacteria obtained from 5S rRNA and 16S rRNA sequence data

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