1
BioSystems, 16 (1983) 1-8
Elsevier Scientific Publishers Ireland Ltd.
NITROGEN FIXATION AS EVIDENCE FOR THE REDUCING NATURE OF THE EARLY
BIOSPHERE*
E . BRODA and G.A. PESCHEK
Institute of Physical Ch'emistry, Vienna University, Austria
(Received February 17th, 1982)
(Revision received September 14th, 1982)
Probably the first nitrogen fixers were anaerobic, non-photosynthetic, bacteria, Le. fermenters. During the
evolution of N, fixation they still needed nitrogen on the oxidation level of ammonia. Because of the complexities in structure and function of nitrogenase this evolution must have required a long time. The photosynthetic
and later the respiring bactet'ia inherited the capacity for N, fixation from the fermenters, but the process did
not change a great deal when it was taken over.
Because of the long need for NH" which is unstable in a redoxneutral atmosphere, a lom~-persisting reducing
atmosphere was needed, The transition to a redoxneutral atmosphere, dominated by CO " H, O and N " cannot
have been rapid, and the NH, in it was recycled. Probably the atmosphere contained for a long time, as was
suggested by Urey but is often denied now, a great deal of methane as a reductant. The recycling occurred with
participation of intermediates like cyanide, through energy input as UV radiation or as electric discharges. A
stationary state was set up.
The hypothesis is recalled that coloured, photosynthetic, NH , bacteria, analogous to coloured sulphur bacteria, may have existed, or may still exist, in reducing conditions. A few remarks are made about the origin of
nitrification in the later, oxidizing atmosphere,
Introduction
..
In this paper the concept will be supported
on biological grounds, namely through
consideration of the evolution of N 2 fixation,
that the early biosphere of the Earth contained appreciable concentrations of nitrogen
on the oxidation level of NH 3 for a long
time. (For simplicity, we sl).all speak below,
where permissible, of NH 3 only.) The early
biosphere is here defined as the place where
life was represented only by anaerobic,
non-photosynthetic, bacteria, i.e. by obligate fermenters. In the view of many authors
such bacteria were the first organisms on
Earth. This "classical" view is also held by
the present authors (Broda, 1978a,b; Broda
and Peschek, 1979; Peschek 1981).
*In honour of the great physical chemist Otto Kratky,
Graz, on his 80th birthday.
The NH 3 was not compatible with an
oxidizing atmosphere, containing 02' Because of the photochemical instability of
NH 3 it was not even compatible with a
redoxneutral atmosphere, i.e. with an atmosphere dominated by H 2 0, CO 2 and N 2 ,
but free of 02' Thus we are led to reaffirm
a further "classical" idea, namely, the idea
of a long-persisting reducing atmosphere
on the early Earth (Oparin, 1924, 1938 ;
Haldane, 1929; Urey, 1952a,b; Hart, 1979) .
We contradict the opposing views recently
expressed by a number of authors, e.g. by
Henderson-Sellers et al. (1980), who went
to the length of claiming that "the concept
of early oxidized atmospheres on the terrestrial planets is becoming the new orthodoxy. "
According to a hypothesis that is independent of our evolutionist arguments the presence of NH 3 in the early (reducing) atmosphere compensated for the lesser luminosity
0303-2647/83/$03.00 © Elsevier Scientific Publishers Ireland Ltd .
Printed and Published in Ireland
2
of the early Sun through a greenhouse effect
(Sagan and MuHen, 1972; Sagan, 1977).
Thus there is no need to assurne a lower
temperature on the early Earth. The required
mixing ratios of NH 3 have been discussed
by Kuhn and Atreya (1979) and by Henderson-SeHers and Schwartz (1980). It was not
stated in these papers that persistence of
NH 3 was needed by organisms, though Sagan
and MuHen mentioned its usefulness.
Reducing, redoxneutral and oxidizing atmospheres
Because of the preponderance of hydrogen
in the solar nebula it is generally assumed
that the very first atmosphere of the agglomerating Earth must have been reducing
and must therefore also have contained
its nitrogen in reduced form. The early
presence of NH 3 is supported by its abundan ce on the big and cold planets Jupiter
and Satum, which unlike the terrestrial
planets did not lose their early atmospheres
(Smith et al., 1980).
(The considerable NH~ content of silicates
in igneous rocks (Wlotzka, 1961; Stevenson,
1962; Honma and Itihara, 1981) unfortunately cannot be used as an argument for the
presence of NH 3 on the early Earth, as long
as it is not demonstrated that not all these
rocks are metamorphic. More attention
should be paid to this problem.).
Most authors think that the primary
atmosphere of the Earth was thin and was
lost rapidly (Brown, 1952). Then the present
atmosphere must be derived from the secondary atmosphere that arose from rocks
through volcanism and other forms of degassing (see Rubey, 1955). This atmosphere
went over, at some time, from a reducing
to a redoxneutral state, and later to an
oxidizing state. Processes contributing to
this change were loss of hydrogen into space,
and later photosynthesis by organisms.
It is often claimed that the transition,
at least from reducing to redoxneutral con-
ditions, was rapid. This is e.g. the view of
Walker (1977, 1978); thus early evolution
of prokaryotes is to have taken place in
absence of bulk quantities of reductants,
i.e. in nearly redoxneutral conditions. Berkner
and Marshali (1967) in their influential
work went even further and suggested that
because. ·of the photolysis of water vapour
already the prebiotic atmosphere was oxidizing. Possible O 2 levels of the order of
0.1 % of the present atmospheric level (P AL)
were mentioned. Recently physical considerations induced Carver (1981) to reemphasize photolytic O 2 production before
photosynthesis. On the basis of biologicalbiochemical as weH as geological-geochemical
data Towe (1978, 1981) likewise supported
a strong role of O 2 from photodissociation
of H 2 0 before the advent of O 2 from plant
photosynthesis. Mineralogical studies led
Dimroth and Kimberly (1976) to the assumption of an oxidizing atmosphere as
early as 3.75 gigayears (Gyr) before now;
for further references to work on ancient
rocks see Towe (1981).
The basis of our opposed view that favours
long persistence of the reducing atmosphere
is that NH 3 (or derivatives) were needed
for the ancient bacteria, and therefore must
have been present before the advent of N 2
fixation, and that the process of N 2 fixation
took a long time to evolve. Thus we disagree with Eugster's (1972) view that any
initial NH 3 in the atmosphere "was oxidized
to nitrogen long before the origin of life".
The case for a long persisting reducing
atmosphere will not be argued here in all
its aspects. The evaluation of all cosmochemical, geophysical, mineralogical, biochemical etc. data goes far beyond the capacity of one working group. Rather it is to
be stated here that the evolution of N 2
fixation, necessarily a lengthy process, was
possible only in the continuing presence
of NH 3 , and therefore required a reducing,
rather than an oxidizing or redoxneutral,
atmosphere. If this argument is valid, it is
decisive by itself.
3
The origin of nitrogen fixation
In the present biosphere organismic nitrogen is typicallyon the redox level of NH 3 •
Amino acids and many other biomoieeules
consist of substituted NH 3 • While the purine
and pyrimidine rings of the nucleotides
formally contain nitrogen at a higher level
of oxidation, they are in fact biosynthesized
from amino acids. Organic derivatives of
nitric oxides are normally found only in the
eukaryotes, Le. in cells of late origin; therefore these substances can be disregarded
here. Thus all life is, and no doubt always
was, essentially based on nitrogen on the
redox level of NH 3 , Le. on nitrogen in the
most strongly reduced form.
Many recent prokaryotes - fermenters,
photo synthesizers and respirers - are capable
of reduction of atmospheric dinitrogen,
i.e. of N 2 fixation. In the present world,
fixation by respirers is observed also in air,
Le. in oxidizing overall conditions. However,
comparative-biochemical considerations show
that N 2 fixation did not arise in an oxidizing
biosphere (Broda, 1975,1978b; Broda and
Peschek, 1980). The machinery for the
process is quite sensitive to 02' and must
therefore in aerobes be specially protected
(Postgate, 1978). Moreover: mere absence
of 02' i.e. a redoxneutral medium, was not
sufficient for N 2 fixation to arise. Reducing
conditions were needed. The reasoning
is as follows.
In all organism the mechanisms for N 2
fixation are so much alike that their monophyletic origin cannot be doubted. In every
case, a complicated enzyme system called
nitrogenase is needed, and this is quite similar
in all N 2 fixers. Further, notwithstanding
the exergonicity of NH 3 synthesis from N 2
and sources of hydrogen on the redox potential level of H 2 a large amount of A TP is
always needed for N 2 fixation by nitrogenase.
This also applies to H 2 release by nitrogenase;
this parallel, wasteful, process is 0 bserved
with all N 2 fixers. Nitrogenase may have
evolved from an ATP-requiring, H 2 releasing,
hydrogenase, likewise sensitive to 02' but the
conversion was not completed, and so release
of H 2 continues (Broda and Peschek, 1980).
The nitrogenase may have arisen in early
fermenters, presumably not so different
from the re cent clostridia. In their time
disposal of H 2 , catalyzed by hydrogenase,
into the atmosphere was, because of its
highly reducing character, still difficult
and required ATP (Broda and Peschek,
1980). The capacity for N 2 fixation later
was inherited by photosynthesizers and,
still later, by respirers. Thus the requirement
for A TP, both for H 2 release and for N 2
fixation, is a relic. It appears that because
of the inherited structure of the enzyme
system the organisms could never get rid of
the requirement for ATP.
In view of the essential identity of nitrogenase in photosynthetic and in respiring
organisms with that in fermenters it must
be concluded that the enzyme system
reached its present composition long before
the atmosphere, as a consequence of plant
photosynthesis, turned oxidizing. Postgate
(1974) put forward an alternative view on
the evolution of the nitrogenase system: after
its origin in some group of bacteria it is
supposed to have spread widely by horizontal
gene transfer, notwithstanding the enormous differences between different bacterial
groups. However this may be, also on this
view the nitrogenase system is monophyletic.
Because of its complexity, the development
of the nitrogenase system must have taken
a long time (Broda, 1977a). As long as the
nitrogenase activity of the ATP-requiring
hydrogenase was not yet sufficient to cover
bacterial needs for reduced nitrogen, an
additional source of NH 3 must have been
available. On the other hand, because of
the heavy expenditure of A TP needed for
N 2 fixation, the nitrogenase system will
not have developed beyond actual needs
as existing at the given biospheric abundance of NH 3 and /or derivatives. We venture
the crude guess that for the emergence
of a reasonably efficient nitrogenase system
4
a time of the order of several hundred megayears was needed.
Production and maintenance of ammonia
Nowadays gases issued by volcanoes are
mostly redoxneutral, and only rarely reducing. However, as long as the differentiation
of the Earth had not gone far yet and the
upper part of the mantle still contained
metallic iron, the outcoming gases may
generaHy have been reducing (Holland,
1962; Hart, 1979). Thus in addition to
H 2 0, CO 2 and N 2 , they may have included
considerable H 2 and NH 3 •
The homogeneous formation of the Earth,
the consequent presence of Fe in the mantle
and therefore the reducing nature of the
early products of degassing have been questioned by Walker (1977,1978), Ringwood
(1979), Schidlowski (1981) and others, who
assume a higher temperature for the early
Earth, and as a consequence rapid differentiation. Nevertheless Walker (1977) admitted
"some" hydrogen and "traces" of NH 3 in
early volcanic gases. In any case, the processes within the early Earth are not yet
known for sure. In their recent review Pollack
and Yung (1980) conclude that rapi.d accretion of the Earth into a completely segregated body is unlikely, and that "sizeable"
amounts of NH 3 may have continued to
be generated.
There may have existed a further source
of NH 3 in addition to degassing, namely
radiation chemistry and photochemistry.
In work without biological implications,
Yokohata and Tsuda (1967) had noted
NH 3 production in the action of silent discharges on mixtures of N 2 and water vapour.
After Schrauzer (1978; see Schrauzer et al.,
1979) had found reduction of N 2 to NH 3 in
presence of water vapour by sunlight in
contact with certain desert sands containing
Ti0 2 and bound Fe it was suggested (Henderson-SeHers and Schwartz, 1980; Chittenden
and Schwartz, 1981) that photochemical
action may have generated much NH 3 also
in early times. While these authors propose
local patches of NH 3 , it appears likely to us
that any NH 3 formed was spread by winds.
The presence of NH 3 from the various
sources made chemical (abiotic) evolution
possible. Indeed NH 3 has been the prtferred
source of nitrogen in experiments for the
simulation of the abiogenesis of biomolecules, beginning with Löb (1913) and, much
more extensively and influentiaHy, with
Miller in 1953 (see Miller and Urey, 1959).
Later, any remaining reduced nitrogen was
available to the eobionts and, subsequently,
to the bacteria.
But the reduced nitrogen could only
have persisted in a reducing, and not in a
redoxneutral, and still less in an oxidizing,
biosphere. As pointed out by Wildt, Hutchinson and Kuiper, NH 3 is easily decomposed
by short-wave UV light (for references to
early work see Rubey (1955)). One oftenquoted estimate is that the mean time of
persistence (mean time required for decomposition) of NH 3 was of the order of 104 years
only · (Abelson, 1966). On the basis of more
detailed considerations Ferris and Nicodem
(1972) computed persistence times of NH 3
about one order of magnitude longer. In
contrast, the most recent work, by Kuhn
and Atreya (1979), led to a far shorter
persistence time of NH 3 , namely, only 10- -40
years, depending on the mixing ratio. In
summary it may be stated that in broadly
redoxneutral conditions the persistence time
of NH 3 gas exposed to UV radiation is always
short. In all these computations the destructive action of electric discharges, wh ich
may weH depress persistence times further,
has not yet been taken into account.
One factor that increased the persistence
time of NH 3 on the Earth was its solubility
in water, with consequent shielding (see
Miller and Orgel, 1974). Short-wave UV is
absorbed by H 2 0, and electric discharges
do not penetrate. It is hard to say what
proportion of the biospheric NH 3 was aqueous, as the solubility strongly depends on the
5
pH value, and this is not known for early
bodies of water. Most of the NH 3 was dis. solved rather than free if the pH value of the
early ocean was similar to that of the present
day: about 8 (Miller and Orgel, 1974). Other
authors think of even lower pH values (Rubey,
1955; Hart, 1978; Wigley and Brimblecombe,
1981), i.e. of still better shielding. A further
protective factor - was adsorption of aqueous
NH; by clay (Bada and Miller, 1966; Miller
and Orgel, 1974); part could be dissolved,
and another part adsorbed.
The overall result is that not even an
approximate value for the persistence time
of NH 3 on a redoxneutral Earth can be
given if shielding is taken into account. But
one wonders whether the persistence time
could have been sufficiently long compared
to the time needed for the evolution of N 2
fixation: as suggested before, of the order
of 10 8 years_ The persistence time would
have had to exceed the values computed
by Ferris and Nicodem (1972) or by Kuhn
and Atreya (1979) for practically unshielded
NH 3 gas, i.e. typically lOs or 10 years, by
factors of the orders of 10 3 or 107, respectively.
Constant replenishment of NH 3 by outgassing in itself would not be sufficient
for the maintenance of a sufficient concentration, as enormous amounts of the
photochemical decomposition product N 2
would accumulate. Reformation of NH 3 was
needed, i.e. the NH 3 had to be recycled.
Recycling was possible only in reducing
conditions.
Backing of ammonia by reductants
When mix ture s of N 2 and reductants
containing hydrogen are exposed to UV or
electric discharges, stationary states must
be set up so that synthesis and destruction
of NH 3 compensate one another. The position
of this stationary state must depend on the
kind and on the intensity of the energy
flux and on the composition of the mixture.
In the atmosphere and hydrosphere of the
early Earth the mixture will also have contained further components, notably CO 2 and CO.
The reaction products will have included
further substances, especially HCN, a possible intermediate in NH 3 synthesis.
An atmosphere with H 2 as the only reductant was hardly good enough. While
the mean escape time of H 2 from the pr imordial atmosphere is not known for certain,
it cannot have been long (see Hart 1978;
Pollack and Yung, 1980). The 1% H 2 conceded to the "primitive" atmosphere by
Walker (1977) is arbitrary, and in any case
that amount of H 2 would, in view of so me
experimental results of Ferris and Nicodem
(1972), not help.
Reformation of NH 3 from CH 4 and its
decomposition products would be more
promising. The presence of CH 4 in the primordial atmosphere was assumed by Urey
(1952a,b). The idea fell into disfavour
among many authors after Rubey (1955)
had argued on geochemical grounds against
the persistence of hydrocarbons on the
early Earth. Walker (1977) also rejected
the idea of bulk quantities of CH 4 • On the
other hand, Cloud (1968) carefully limited
his rejection of an atmosphere rich in CH 4
or NH 3 to the time from about 3 gigayears
before now (1.6 gigayear from the origin of
the Earth), i.e. a reducing atmosphere of this
kind was not excluded for the earlier period
that alone is under discussion here. Hart
(1978,1979) argued that the early atmosphere contained CH 4 until this was oxidized
away 2 gigayears aga by O 2 from plant
photosynthesis. According to that author,
the persisting presence of gaseous re ductants is in fact needed to account for .missing
O 2 from photosynthesis. Gold and Soter
(1980) suggested that enormous amounts
of CH 4 of primordial, abiotic, origin are
still locked in the deep part of the Earth 's
crust.
CH 4 presumably was also produced by
anaerobic, non-photosynthetic, bacteria (Ycas
(1972). The methane bacteria that make
CH 4 from CO 2 and H 2 are much studied
6
now and are considered as particularly ancient
by many authors (Woese and Fox, 1977).
These organisms often occur in association
with H 2 producing fermenters so that they
do not depend on H 2 in the atmosphere.
The symbiotic system formerly known as
Methanobacterium omelianskii is a weH
known example (Bryant et al., 1967).
The simultaneous presence of CH 4 and
N 2 could lead to the production of NH 3
via reactions exemplified by Eqns. 1-3.
The values of t::,. Go are computed from the
tables of Burton (1957) and Kortüm (1960),
and apply in the presence of liquid water.
CH 4 + N 2 = CN- (aq) +
NH~
(aq);
t::,.G o = 138 kJ
(1)
CH 4 + N 2 + H 2 0 = 2NH 3 (aq) + CO;
t::,.G o = 97 kJ
(2)
or
or
CH 4 + N 2 + 2H 2 0 = HCOO- (aq)
+ NH: (aq) + NH 3 (aq);
t::,.G o =
72 kJ
(3)
While the equilibria lie on the left, the reactions could be forced to the right by
energy input as UV light or electric discharges. The hydrolytic synthesis of NH~
from CN- is, in contrast, exergonic:
W (pH 8) + CN- + 2H 2 0
HCOO- + NH:;
t::,.G o = -80 kJ (4)
=
Indeed reactions of these and similar
kinds were observed by many authors, e.g
Miller (1957) and Sanchez et al. (1966),
on application of sparks to reducing systems
(see Lazcano-Araujo and Or6 1981). Nitrogen initially fixed in electric discharges in
the presence of H 2 0 as nitrite or nitrate
(Yung and McElroy, 1979; Zohner and
Broda, 1979) would in reducing conditions
also provide NH 3 • According to computations
by Hart (1978,1979) the early, CH 4 containing atmosphere may have contained one
thousandth of its nitrogen as NH 3 , and this
was lost, along with the CH 4 , only after
the advent of plant photosynthesis.
As the biosphere gradually turned redoxneutral, the abundance of NH 3 must have
decreased_ · But N 2 fixation tended, after it
had arisen in fermenters, to stabilize the abundance, and biospheric NH 3 may even have
increased at some stage or other. In contrast,
photosynthetic bacteria may have existed
that obtained ATP from the photochemical
oxidation of NH 3 by CO 2 , just as the coloured
(purple or green) sulphur bacteria oxidize
H 2 S by CO 2 • Such "coloured ammonia
bacteria" have not yet been found, and
they may be extinct; however, the existence
of nitrificants (see below), possibly derived
from coloured ammonia bacteria, may point
to their existence at least in the past (Broda,
1977b).
In our view, oxidizing coriditions began
only after the invention of plant photosynthesis by ancestors of the present bluegreen algae (cyano bacteria). In the presence
of O 2 ammonia is unstable. The oxidation
of NH 3 or of other organic compounds
containing nitrogen at the oxidation level
of NH 3 by O 2 to N 2 , nitrite or nitrate is highly
exergonic. The oxidation of NH 3 may occur
abiotically, through fires, lightning, etc.
Another part is oxidized by nitrificants to
nitrite and nitrate in respiratory processes,
with concomitant oxidative phosphorylation
(see Broda, 1978a). The NH 3 needs of cells
are now covered by the assimilatory reduction of nitrite and nitrate.
In the last analysis, the resulting metabolic
wheel is driven by solar energy, as has been
discussed elsewhere (Delwiche, 1970; Broda,
1978b). The wheel, lubricated by the needed
enzyme systems, moves the nitrogen cyclically through its three valency states.
Acknowledgement
We thank A.W. Schwartz for useful critical
7
remarks, especially in connection with the
role of cyanide.
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