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Protein structure and the molecular evolution of biological energy conversion
BioSy.stems 6 (19’75) 217-223 0 North-Holland Publishing Company, Amsterdam - Printed in The Netherlands
XflRICK Department
x
BALTSCHEFFSKY of Biochemistry,
Arrhenius Laboratory
uetion
Already half a century version of Prdskhozhden
University of Stockho1m.SI04
05. Stockholm,
cular origin and essenc between nucleotide an
Sweden
218
time
T 1
I
iB
la
Fig. 1 j O-iigin and early evolution of life. (la) Monophyletic origin; (1 b) diphyletic (as an example of poly phyletic) origin.
ganic polyphosphates were suggested, by Kulaev (19,20), as such early energy-rich phosphates, based upon his important resuits with enzyme reactions of bacterial glycolytic systems. With respect to the electron transport part of MoIogical electron :;ransport phosphorylation systems, I have very recently proposed a hypothesis for the ox-&in and evolution of electron transI9ox-t chains biological
rep%kation as well as translation, as expressed primarily in amircs acid sequence of formed peptide. Qn the other hand, the possibility that present-day organisms should trace their ancestry back to a situation with parallel origin and early evolution of more than one such system, all based on the same nucleotide-peptide principle, should not be excluded (Fig. ), as will be discussed below. ents
0th of the alternatives mentioned above are of immediate interest in coenection with some new and very rapid developments relating to the field of molecul !3ioslogicd energy conversion. progress occurring at the level of protein cture it will be necessary to present as a nd some other recent developments. (llJ2) has pioneered the more de-
o, found bioch
thus formed
(22).
elo
219
mination of proLteins, by Rossmann and his group (24,26), Branden and his group (26), Watson and his group (27), Schulz and his group (28), Blake and Evans (29), and many others, a new molecular pattern of protein structure is beginning to emerge. This would appear to allow soon a deeper understanding of both evolution and mechanism in biological energy conversion. Indeed, it appears to amount a new integration at the level of polypept~de structure and function over large of the entire field of biological ener t to the evolution and funcsecondary st~~tura~ features
e ~~mrno~ ancestry in differ-
and evolution transport
of proteins
in electron
The biochemical unity of metabolism is a well-known concept, long realized from investigations of relatively simple organic molecules, such as substrates and products, coenzymes and prosthetic groups, p~i~~~at~ng in the reactions of living cells. More recent studies, at the level of protein structure, have trees for sever chrome c (33) an Certain bacterl
support of (3) is still very weak (22,23). Rae and Rossman (3) discovered similar super-secondary struciures or domains in an FMN-containing flavoprote-ml, Clostridiuti MP flavodoxin, and an NAD-binding proteei;l, lactate dehydrogenase (LD) from dog-fish. Such a domain consists of about 60 amino acids forming a three standard parallel P-pleated sheet with connecting ar-helices. This occurs once in flavodoxin, whic:h binds a mononucleotide and twice in LD, which binds a dinucleqtjde. ‘The fact that a rather similar domain also was found in subtilisin lead to their assumption that this structural similarity was an expression of functional convergence rather
costarred ~y~~rn~di~es, and that coded for poly;?eptides in wh
a hi se sequences
ducing suitable P-sheet structures, may have given the very type of polypeptide secondary structure which has nucleotide binding property! Nucleotide binding may thus have evolved very early, either separately, or in ancestral relationship with the binding of iron-sulfur clusters. In other words (compare Fig. l), is there a mono- or a di-phyletic molecular origin of biological electron transport? Both these alternatives appear much more attractive and probable today than a third alternative that does not reckon with any evolutionary relationship at all between different groups of proteins. Although the whole spectrum of alternatives should perhaps still be considered, I tend to believe that a common ancestry may eventually be traced for ah ‘fivoived in Melogical rt,=*n+ures UbL polypeptide electron transport, as well as many: and possibly even most, other polypeptide startles of living cells. Determination of primary structures also continue to be extremely i
221
can only be imaginea st the present time. It may suffice here to cite Blake and Evans (29): “The possibility of an evolutionary relationship in the nucleotide binding units of two such important groups of enzymes as the dehydrogenases and the kinases, further suggests that other classes of enzymes may also contain this basic unit. The observed specificity of the unit is apparently for the adenosine up of the co-fact oup occurs not y in NAD and also in flavinadenine dinucleotide, and, as the 3’ - phosphate, in co-enzyme A. In view of the present results, it seems possible that the presence of adenosine in these four i may be a cons
well as reaction mechanisms, in biological electron transport an phosphorylation. first concerns electro transport, the sfxon electron transport phosphorylation and the pre-nucleotide level, and the third electron transport phosyho.!ylation of I. Investigation of the st bilized succinate dehydrogenase from bovine heart (44,45) and Rhodospirillum rubrum chromatophores (46). e enzyme contains, on the same ~olypepti inding sites for the
yet been sol~b~ized final reaction in li
222
upon this compl~mentarity and upon the assumption :;hat both members of the proposed RNApolypeptide complex can act as pximordial “polymerases” for one another. ferences zhizni” (“Origin 1. Oparin, A.I., “Prolskhozhdenie of I.&“), Izd, Moskovskii rabochii, Moskva, 1924. 2. Crick, F.H.C., J. Mol. Biol. 38, 367 (1968). 3. Orgel, L.E., J. Mol. Biol. 38, 381 (1968). “The Molecular Biology of the 4. Benjamin, Inc., New York, 1970. aften 58, 465 (1971). 5. ‘@&en, M., Naturwlsse ophyr. 4, 149 (1971). 6. Eigen, M., Quart. Re S., Quart. Revs. Biophys. 4, 213 7. Spiqelman, 1). I, LE., Israel J., Chem. 10, 287 (1972). 8. s, D.R., F.R. Kramer and S. S@iegelman, Sci9. ence 3 80,916 (1973). 10. Miller, S.L. and LE. Orgel, “The Origins of Life on the Earth,” Prentice-Hall, Inc., Englewood Cliffs, 1974. Broda, E., Prop. Biopbys. Mol. Biol. 21, 143 lecular Evolution,” Vol. 2 (E. ), p. 224, North-Holland, AmsterI.am, 1971. Bnltsclleffsky, ., Acta Chem. &and. 21, 1973 (1967). fsky, H., “Molecular Evolution,” Vol. 1 t and C. Ponnamperuma~ eds.), p. 466, cslland, Amsterdam, 1971. Baltscheffsky, H., L-V. von Stedingk, H.-W. Heldt and M. Klingenbe.rg* Science 153, 1120 (1966).
24. Rossmann, M.G., D. Moras and K.W. Olsen, submitted to Nature. M.G., New Scientist 6’1, 266 (1974). 25. hasmann, T. 26. Branden, C.-I., Ii. Ekland, B. Nordstriim, Boiwe, G. Saderland, E. Zeppezauer, I. Oh&son and A. Akzrson, Proc. Nat. Acad. Sci, U.S. 70, 2439 (1973). 27. Bryant, T.N., H.C. Watson and P.L. Wendell, Nature 247,14 (1974). 28. Schulz, G.E., M. Elzinga, F. Marx and R.H. Schirmer,, Nature 250,120 (1974): 29. Blake, C.C.F., and P.R. Evans, J_ Mol. Biol., in press. J. Mol. Biol. 76, 30. Rao, S.T., and M.G. Ro 241(1973). ~r~emien,” i 31. Berzelius, J.J., ‘“Fiirel Vol. 1, p. 3, Carl Delen, S~ck~olm, 1806. 32. Darwin, C., “On the Origin of Speci and 11s;ardor, 1860. 33. Fitch, WM. and E. Mar~ol~~, Science 155,279 .(1967). 34. Dayhoff, MO., “Atlas of Protein E&pen Structure,” Vol. 5, p. 392, The National dical Research Foundation, Silver S 35. Hall, D.O., R. Cammack and K.K. 233,136 (1971). 36. Hall, D.Q., R. Cammack and and Experiment in Exobi Schwartz, ed.), pp_ 6737. 38. 39.
40. 41. oc. Nat. Acad. Sci. U.S. 42.
mp. Biol. 19, 246
urn,
Abstracts, no. 368,
43.
223
49. Kiemme, J.-H., and H. Gest, Eur. J. Biochem. 22, 529 (1971). 50. Beechey, R.B., and K.J. Cattell, Cur. Top. energ., 5, 305 (1973).
51.
Baitscheffsky, H. and M. ~~~c~effsky, v. Bioehem. 43, 871 (1974).
Ann.
XflRICK Department
x
BALTSCHEFFSKY of Biochemistry,
Arrhenius Laboratory
uetion
Already half a century version of Prdskhozhden
University of Stockho1m.SI04
05. Stockholm,
cular origin and essenc between nucleotide an
Sweden
218
time
T 1
I
iB
la
Fig. 1 j O-iigin and early evolution of life. (la) Monophyletic origin; (1 b) diphyletic (as an example of poly phyletic) origin.
ganic polyphosphates were suggested, by Kulaev (19,20), as such early energy-rich phosphates, based upon his important resuits with enzyme reactions of bacterial glycolytic systems. With respect to the electron transport part of MoIogical electron :;ransport phosphorylation systems, I have very recently proposed a hypothesis for the ox-&in and evolution of electron transI9ox-t chains biological
rep%kation as well as translation, as expressed primarily in amircs acid sequence of formed peptide. Qn the other hand, the possibility that present-day organisms should trace their ancestry back to a situation with parallel origin and early evolution of more than one such system, all based on the same nucleotide-peptide principle, should not be excluded (Fig. ), as will be discussed below. ents
0th of the alternatives mentioned above are of immediate interest in coenection with some new and very rapid developments relating to the field of molecul !3ioslogicd energy conversion. progress occurring at the level of protein cture it will be necessary to present as a nd some other recent developments. (llJ2) has pioneered the more de-
o, found bioch
thus formed
(22).
elo
219
mination of proLteins, by Rossmann and his group (24,26), Branden and his group (26), Watson and his group (27), Schulz and his group (28), Blake and Evans (29), and many others, a new molecular pattern of protein structure is beginning to emerge. This would appear to allow soon a deeper understanding of both evolution and mechanism in biological energy conversion. Indeed, it appears to amount a new integration at the level of polypept~de structure and function over large of the entire field of biological ener t to the evolution and funcsecondary st~~tura~ features
e ~~mrno~ ancestry in differ-
and evolution transport
of proteins
in electron
The biochemical unity of metabolism is a well-known concept, long realized from investigations of relatively simple organic molecules, such as substrates and products, coenzymes and prosthetic groups, p~i~~~at~ng in the reactions of living cells. More recent studies, at the level of protein structure, have trees for sever chrome c (33) an Certain bacterl
support of (3) is still very weak (22,23). Rae and Rossman (3) discovered similar super-secondary struciures or domains in an FMN-containing flavoprote-ml, Clostridiuti MP flavodoxin, and an NAD-binding proteei;l, lactate dehydrogenase (LD) from dog-fish. Such a domain consists of about 60 amino acids forming a three standard parallel P-pleated sheet with connecting ar-helices. This occurs once in flavodoxin, whic:h binds a mononucleotide and twice in LD, which binds a dinucleqtjde. ‘The fact that a rather similar domain also was found in subtilisin lead to their assumption that this structural similarity was an expression of functional convergence rather
costarred ~y~~rn~di~es, and that coded for poly;?eptides in wh
a hi se sequences
ducing suitable P-sheet structures, may have given the very type of polypeptide secondary structure which has nucleotide binding property! Nucleotide binding may thus have evolved very early, either separately, or in ancestral relationship with the binding of iron-sulfur clusters. In other words (compare Fig. l), is there a mono- or a di-phyletic molecular origin of biological electron transport? Both these alternatives appear much more attractive and probable today than a third alternative that does not reckon with any evolutionary relationship at all between different groups of proteins. Although the whole spectrum of alternatives should perhaps still be considered, I tend to believe that a common ancestry may eventually be traced for ah ‘fivoived in Melogical rt,=*n+ures UbL polypeptide electron transport, as well as many: and possibly even most, other polypeptide startles of living cells. Determination of primary structures also continue to be extremely i
221
can only be imaginea st the present time. It may suffice here to cite Blake and Evans (29): “The possibility of an evolutionary relationship in the nucleotide binding units of two such important groups of enzymes as the dehydrogenases and the kinases, further suggests that other classes of enzymes may also contain this basic unit. The observed specificity of the unit is apparently for the adenosine up of the co-fact oup occurs not y in NAD and also in flavinadenine dinucleotide, and, as the 3’ - phosphate, in co-enzyme A. In view of the present results, it seems possible that the presence of adenosine in these four i may be a cons
well as reaction mechanisms, in biological electron transport an phosphorylation. first concerns electro transport, the sfxon electron transport phosphorylation and the pre-nucleotide level, and the third electron transport phosyho.!ylation of I. Investigation of the st bilized succinate dehydrogenase from bovine heart (44,45) and Rhodospirillum rubrum chromatophores (46). e enzyme contains, on the same ~olypepti inding sites for the
yet been sol~b~ized final reaction in li
222
upon this compl~mentarity and upon the assumption :;hat both members of the proposed RNApolypeptide complex can act as pximordial “polymerases” for one another. ferences zhizni” (“Origin 1. Oparin, A.I., “Prolskhozhdenie of I.&“), Izd, Moskovskii rabochii, Moskva, 1924. 2. Crick, F.H.C., J. Mol. Biol. 38, 367 (1968). 3. Orgel, L.E., J. Mol. Biol. 38, 381 (1968). “The Molecular Biology of the 4. Benjamin, Inc., New York, 1970. aften 58, 465 (1971). 5. ‘@&en, M., Naturwlsse ophyr. 4, 149 (1971). 6. Eigen, M., Quart. Re S., Quart. Revs. Biophys. 4, 213 7. Spiqelman, 1). I, LE., Israel J., Chem. 10, 287 (1972). 8. s, D.R., F.R. Kramer and S. S@iegelman, Sci9. ence 3 80,916 (1973). 10. Miller, S.L. and LE. Orgel, “The Origins of Life on the Earth,” Prentice-Hall, Inc., Englewood Cliffs, 1974. Broda, E., Prop. Biopbys. Mol. Biol. 21, 143 lecular Evolution,” Vol. 2 (E. ), p. 224, North-Holland, AmsterI.am, 1971. Bnltsclleffsky, ., Acta Chem. &and. 21, 1973 (1967). fsky, H., “Molecular Evolution,” Vol. 1 t and C. Ponnamperuma~ eds.), p. 466, cslland, Amsterdam, 1971. Baltscheffsky, H., L-V. von Stedingk, H.-W. Heldt and M. Klingenbe.rg* Science 153, 1120 (1966).
24. Rossmann, M.G., D. Moras and K.W. Olsen, submitted to Nature. M.G., New Scientist 6’1, 266 (1974). 25. hasmann, T. 26. Branden, C.-I., Ii. Ekland, B. Nordstriim, Boiwe, G. Saderland, E. Zeppezauer, I. Oh&son and A. Akzrson, Proc. Nat. Acad. Sci, U.S. 70, 2439 (1973). 27. Bryant, T.N., H.C. Watson and P.L. Wendell, Nature 247,14 (1974). 28. Schulz, G.E., M. Elzinga, F. Marx and R.H. Schirmer,, Nature 250,120 (1974): 29. Blake, C.C.F., and P.R. Evans, J_ Mol. Biol., in press. J. Mol. Biol. 76, 30. Rao, S.T., and M.G. Ro 241(1973). ~r~emien,” i 31. Berzelius, J.J., ‘“Fiirel Vol. 1, p. 3, Carl Delen, S~ck~olm, 1806. 32. Darwin, C., “On the Origin of Speci and 11s;ardor, 1860. 33. Fitch, WM. and E. Mar~ol~~, Science 155,279 .(1967). 34. Dayhoff, MO., “Atlas of Protein E&pen Structure,” Vol. 5, p. 392, The National dical Research Foundation, Silver S 35. Hall, D.O., R. Cammack and K.K. 233,136 (1971). 36. Hall, D.Q., R. Cammack and and Experiment in Exobi Schwartz, ed.), pp_ 6737. 38. 39.
40. 41. oc. Nat. Acad. Sci. U.S. 42.
mp. Biol. 19, 246
urn,
Abstracts, no. 368,
43.
223
49. Kiemme, J.-H., and H. Gest, Eur. J. Biochem. 22, 529 (1971). 50. Beechey, R.B., and K.J. Cattell, Cur. Top. energ., 5, 305 (1973).
51.
Baitscheffsky, H. and M. ~~~c~effsky, v. Bioehem. 43, 871 (1974).
Ann.