Effects of UV selection pressure on evolutionary development patterns of early organism

Sagan, C.

English

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OCT 1971
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Center for iadrophysZcs and Spy ear c h
ITHACA, N.Y.
CORNELL UNIVERSITY
CENTER FOR RADIOPHYSICS AND SPACE RESEARCH
Ithaca, N.Y.
May 1971
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CRSR 445
ULTRAVIOLET SELECTION PRESSURE ON THE
EARLIEST ORGANISMS
Carl Sagan
Laboratory for Planetary Studies
Cornell University
Ithaca, New York .14850
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Abstract
An examination of the probable photochemistry of the
primitive reducing atmosphere of the Earth reveals a window,
approximately bounded at 2400 A to short wavelengths by H2S,,
0
and possibly at 2700-2900 A to longer wavelengths by aldehydes.
The solar ultraviolet flux in this 2600 A window, delivered to
unprotected organisms at the surface, corresponds to a contemp-
orary mean lethal dose in t 0.3 seconds. Extreme selection
pressure for ultraviolet protection must have come into being.
In addition to the early evolution of pyrimidine dimer ligases,
catalase and peroxidase reduction mechanisms, and photoreactiv-
ation, it is suggested that two evolutionary paths developed.
In one, heter.,gtrophs lived below the oceanic thermocline and
are suggested as perhaps the ancestors of the prokar-yotes .
In the other, organisms living near the oceanic surface sur-
roundedunded themselves with ultraviolet absorbing layers of purines
and pyrimidines. The resulting organisms have dimensions of
tens to hundreds of microns and are sugge :ted to be the ances-
tors of the eukaryotes
	
Subsequent specialization of this
initially inert shielding, e.g., into ribosomal RNA, may have
occurred.
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Some years ago T proposed that uv light, partially pene-
trating the primitive reducing atmosphere of the Earth, posedX
a major problem for the earliestevolution of life (1). This
argument can now be updated and refined. We adopt the by now
traditional picture of a secondary reducing atmosphere, from
which an excess of hydrogen has already escaped to space, at
a total surface pressure N 1 bar. The predominant constitu-
ents, methane, ammonia, water vapor, CO, N 2 , H 2 , and the noble
gases are all perfectly transparent for these pressures at
0
wavelengths a> 2200 A. Hydrogen sulfide is another probably
important constituen< of the primitive terrestrial atmosphere:
it is the thermodynamically stable sulfur-containing gas under
reducing conditions, and is even today a volcanic effluent.
Holland (2) estimates that the volume mixing ratio of H 2  in
the first stage of the evolution of the Earth was between
10-2 and 10 -4 ; that is, 'L 10 2 to 10 4 cm-atm H 2 S (1 cm-atm
of gas = a columnar density of Loschmidt's number of molecules,
3 x 10 19 molecules cm- 2 ) . But this is are estimate made ` while
ignoring photochemical degradation, which we know is very
efficient; in fact the photolysis, of H2  may itself k^,ave played
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a very major role in the prebiological formation of org"'c
compounds (3). From the laboratory absorption spectrum of
H 2 S M., which shows tha absorption coefficient to decline
0	 0
approximately I order of magnitude every 100 A below 2400 As
it appears likely that H 2 S, contributed negligible opacity on
0	 0
the primitive Earth at a> 2100 A	 2600 A (cf. Fig. 1) .
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Accordingly, a significant ultraviolet window appears to have
existed at A 2400 A, tempered only by intermediate oxidation
state products produced by the photochemistry of the principal
constituents. By far the most abundant such absorbers are the
aldehydes; formaldehyde and acetaldehyde have been detected
in the gas phase in a number of simulation experiments (5) .
Indeed the aldehydes are known intermediaries in the prebio-
logi cal organic synthesis of both sugars and amino acids. The
ultraviolet absorption spectra (6) of formaldehyde and acetal-
0	 o
dehyde are shown in Fig. 1. Between 2400 A and 2900 A the
molar extinction coefficients have values of several dimension,
less units, corresponding to a molecular cross-section a of
the order of 10 -20 Cm2 . Thus optical depths T ti 1 are achieved
with a columnar density of 102 0 molecules cm-2 , which in turn
corresponds to ti 3 cm-atm or N 3 ppm. Models of solar evolution
place the Sun about half a b olometric magnitude fainter 4 x 109
years ago than it is today; but the resulting uv flux can be
calculated to be only slightly less than it is today	 (7). With
such a flux, typical unprotected contemporary organisms -- both
eucaryotes and procaryotes -- acquire a mean lethal dose [cf.
a	 O
ref. (8) ] of ultraviolet radiation at a< 2900 A in < 0. 3 sec.r
Unacceptably high mutation rates will of course occur at much
lower uv doses, and even if we imagine primitive organisms
having much less stringent requirements on the fidelity of
replication than do contemporary organisms, we must require
very substantical uv attenuation for the early evolution of
life to have occurred. This is especially true if we imagine
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contemporary uv-protection mechanisms -- such as pyrimidine
dimer 11gases, photoreactivation, catalase, and the peroxidases --
to have been absent.
In the following discussion we assume that in some manngr
0	 0
or other the incident uv flux between 2400 A and 2900 A had to
be attenuated by a factor ti 10 9 , corresponding to T ti 20. For
T ti 20 to be provided by aldehydes, they must have constituted
ti 100 ppm in the primitive atmosphere. Again, precisely because
aldehydes absorb uv light so readily, they are irreversibly
broken down Lito other phutoproducts. From the aldehyde cross.-
sections of Fig. 1 1 it is easy to calculate that the mean
lifetimes of such molecules in the primitive uv radiation field
were a few hours. For an equilibrium. abundance as high as 100
PPM, the production rate would have had to be ti 3 x 10 17 moler
cubes em-2 sec-1 , which appears to be excessive by a large
factor.	 The situation is quite similar to the contemporary
ozone photochemistry in the Earth's atmosphere, where the photo-
chemical equilibrium abundance is only 10 -1 to 10-2 ppm. How-
ever ozone absorbs much more strongly than the aldehydes in
this wavelength region. Acetone and higher ketones have slightly
0
larger absorption coefficients at A> 2400 A than do aldehydes
(6). but their abundance in the primitive atmosphere should have
been much smaller; indeed, to the best of my knowledge, they
have never been reported in prebiological organic chemistry
simulation experiments. Benzene and polycyclic aromatic hydro-
carbons also absorb in the region of interest, but their gas
phase abundance in the primitive atmosphere is expected to be
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much smaller yet.
While it is clear that there remain many uncertainties
,
about so remote a question as the composition of the primitive
terrestrial atmosphere, it does appear that a significant
0	 0
window existed between 2400 A and 2900 A. Because of the
shapes of the 11 2S and aldehyde absorption spectra (see Fig.
1) the largest window appears to have been in the vicinity of
0
2600 A. But this is precisely the vicinity of peak absorption
by the nucleic acids. In the absence of repair the absorption
of a single ultraviolet photon by the genetic material can be
lethal. Repair mechanisms cannot be expected to have been as
efficient in primitive times as they are today; and even today
they are far from 100% efficient. Photoreactivation, for
example, is N 50% efficient. Thus the earliest self-replicating
polynucleotides must have faced severe selection pressures to
avoid uv damage. The development of enzymatic systems such as
catalase and the peroxidases to undo uv-induced oxidations may
have been developed very early (1); and the microbodies or
peroxisomes of eucaryotes may date from very ancient times.
But 1,n general there are only two efficient solutions to
^j	 the primitive uv hazard: sequestering and shielding. 'Liquid
water absorbs in the 2400 A to 2900 A region, but with quite
low absorption coefficients. Several tens of meters of pure
liquid water are required for significant attenuation of the
incident ultraviolet flux, and I proposed that some of the
earliest living systems may have developed entirely in the
abyssal depths (1). Of course the primitive soup in which
414
the origin of life occurred was not pure liquid water, and many
uv absorbers can be expected to have been present. High molec^
ular weight uv- and visible-absorbing polymers, still unident-
ified in composition, are a pervasive component of experiments
in nrebiological organic chemistry [e.g., ref. (3)]. Thus,
unprotected organisms could have developed much closer to the
surfac.e than tens of meters. But they then ran the risk of
being carried, by slow oceanic convection, to the very tops of
the oceanic surface where the uv dose becomes intolerably high.
The great advantage of a depth of some tens of meters is that
it begins to approach the oceanic thermocline, below which
there is much less effective convective transport to the surface
than from higher levels. We can imagine primitive anaerobic
heterotrophs evolving in the abyssal depths, safely protected.
from the uv flux characteristic of the surface layers, and
metabolizing the variety of organic compounds produced higher
up and carried by convection and molecular and eddy diffusion
to their depth. I propose that these simple abyssal organisms
were the precursors of the prokaryotes.
On the other hand the ;supply of abiogenic food-stuffs
r (and visible light) must have been very much larger nea p the
surface, and an organism adequately shielded from the intense
uv flux would have discovered a very rich and untenanted
ecological niche there. The most suitable shielding material
would seem to hs,ve been purine and: pyrimidne b ases -- the
very source of the uv lability of nucleic acids. These mater,
ials have extremely high absorption coefficients between
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2400 A and 2900 A and are known to have been produced efficiently
in the early history of the Earth (9). 1 propose that another
solution to the uv selection dressure was for the genetic mater-
ial to surround itself with bases or nucleotides having no
function whatever in replication or protein synth;sis. Typical
molar extinction coefficients for purines and pyrimidines, for
nucleotides, and for the nucleic acids themselves are 6 to 8 x 104,
corresponding to a N 3 x 10--16 cm2 (10), a very high value. An
equimolar mixture of the five biologically most common purines
and pyrimidines produces an approximately flat net absorption
spectrum between 2 2400 Aand 2900 A. Considering the crudeness
of this calculation we neglect all hypochromic and solvent effects;
they vary the absorption coefficient characteristically by ti 50%.
The aromatic and heterocyclic amino acids also absorb in this
region and might have played a protective function; but their molar
extinction coefficients are less than the purines and pyrimidines
by factors of about 30; and the laboratory experience in prebio-
logi cal organic chemistry indicates that tryptophan, e.g., is
made much less abundantly than adenine. 	 We assume that a
few percent of the total wel_ght of the shielded cell was in
polynucleotide shielding; this is roughly the same value as the
fractional weight of RNA in both procaryot c and eucaryot c
cells (11). If the shielding comprised several 'tens of percent
by mass, correspondingly smaller cells are implied. It is then
easy to calculate that a cell so protected would have to be
roughly 20 p in radius to achieve T	 1, and 400 p in radius to
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achieve T $ 20, in the absence of any atmospheric or solution
shielding. But the characteristic dimensions of the simplest
eukaryotes, the higher protists, are also between a few U and
a few hundred u (12) . 1 therefore suggest that while the pro,
karyotes developed at abyssal depths, the eukaryotes developed,
at a somewhat later time, near the surface of the waters and
with an ultraviolet umbrella of purines and pyr .midines . A
number of the differences between prokaryotes and eukaryotes are
consistent with this picture; for example, the eukaryotic genetic
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material is carefully maintained within the nuclear membrane
and near the center or most uv-inaccessible region of the cell;
prokaryotes, which in any case fall short by several orders of
magnitude in meeting our protection criterion, appear to have
their DNA strands anchored near the periphery on the cell
	
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membrane (13) . Contemporary eukaryotes are probably not much
better shielded from uv than are contemporary prokaryotes, nor
are their nuclei surrounded by Layers of passively functioning
purines and pyrimidines and their compounds. But a great deal
of evolution has obviously occurred since the earliest times we
are discussing, and it is even possible that cytoplasmic nucleic 2
acids, which originally played a protective role, eventually
developed under the action of uv into performing other functions,
including the rib osomal apparatus (14) . The fact (15) that ^I
major fractions of the ribosomal RNA can be enzymatically
digested away without significantly impairing ribosomal func-
tion suggests that ribosomal RNA may be an evolutionary relic
from times when it played other functions. Otherwise we could
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imagine ribosomal proteins rather than RNA providing all the
structural links between enzymatically active ribosomal sites.
The very early evolutionary path proposed here is not necessar-
ily inconsistent with the idea of a prokaryote endosymbiont
origin of eukaryotes (16); the abyssal and surface populations
could not but have maintained genetic content.
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REFERENCES
C. Sagan, Evolution 11, 40 (1957); C. Sagan, Rad. Res.
15, 174 (1961),
H.D. Holland (1962), In "Petrologic Studies	 A Volume to
Honor A.F. Buddington," Geol.og. Soc. America, N.Y., p, 447.
(3) C. Sagan and B. N. Khare, Science, in press (1971).
(4) E. D. Schultz, A. C. Holland, and F. F. Marmo (1965),"A
congerie of absorption cross- sections for X< 3000 A, " GCA
Corp. Rept . NASA CR--15 .
(5) S. L. Miller (1957), Ann. New York Acad, Sci., 69, 260;
C. Sagan and S. L. Miller, Astron. J. 63, 499 (1760).
(6) J. G. Calvert and J. N,, Pitts (1966), "Photochemistry",
John Wiley and Sons, N. Y.
(7) C. Sagan (1965), in S. W. Fox, ed., "The Origins of Prebio-
logical Systems," Academic Press, New York, p. 238.
(8) A. Hollaender, Ed. (1955), "Radiation Biology," 2, esp.
chaps. 8 and 10 (New York: McGraw Hill).
(9) S. L. Miller and L. E. Orgel (1972), "The Origin of Life,"
(Prentice Hall: Englewood Cliffs, N. J.) 	 To be published,	 k
(11) W. R. S strom, "Microbial life" (1969) , Holt Reinhart and
Winston, N. Y. 2nd ed; K. C. Atwood (1971)s Private
1
communication.
(12) Ra Y. Stanier, M. Doudoroff, and E. A. Adelberg (1963),
"The Microbial World" Prentice-Hall, Inc. Englewood
Cliffs, New Jersey ,.  2nd- ed. ,  p. 140.
1
F x>	 (13) M. R. J. Salton, (1968) "Microbial Cytology" Vol. 23 of
"Comprehensive Biochemistry," M. Florkin and E. M. Stotz,
eds . Elsevier, Amsterdam, Chap. 5.
(14) C. Sagan and P. Shapsh.ak, submitted to J. Theoret. Biol.(1971).
(15) A. Rich, private communication (1971)
1
(10) R. L. Sinsheirner (1955), "Ultraviolet absorption spectra"
Chapter. 5, in "Radiation Biology," 2, A. Hollaender, ed.
McGraw-Hill, New York; A. D. McLaren, and D. Shugar (1964),
"Photochemistry of Proteins and Nucleic Acids," New York,
McMillan; C. Sagan, Science, 159, 4118 (1968) .
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(16) See, e.g., L, Sagan (1967). J. Theoret. Biol. 14, 225;
L. Margulis (19 70)	 "Origin of Eukaryoti c Cells ,"
Yale University Press, New Haven.
(17) This research was supported in part by NASA Grant NGR
33-010-101. 1 am indeb ,zed to Paul Shapshak for several
stimulating discussions, and to K. C. Atwood and Leslie
Orgel for helpful criticism.
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rFigure 1. Ultraviolet absorption cross-sections as a
function of wavelength for H 2S and the two simplest aldehydes.
For' reasonab'le abundances of these gases in the primitive
atmosphere, a significant 2400 	 - 2700 W ultraviolet window
is implied.
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Figure I.


Ultraviolet selection pressure on the earliest organisms

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