FRONTIER RESEARCH ON EARTH EVOLUTION, VOL. 2
Evolution of the atmospheric oxygen in the early Precambrian:
An updated review of geological “evidence”
Kosei E. Yamaguchi1, 2
1 Research
2 NASA
Program for Paleoenvironments, Institute for Research on Earth Evolution (IFREE)
Astrobiology Institute
"... models or working hypotheses that have become widely accepted as organizing principles for the field ... may lead us to ask the wrong
questions ... or disregard significant lines of evidence simply because they seem inconsistent with our model-dependent predictions."
J.W. Schopf, in Earth's Earliest Biosphere
1. Introduction
ic O2 content would have been very low [Kasting and Walker,
1981; Kasting, 1993].
The onset of global oxygenation in the atmosphere-hydrosphere system in the early history of the Earth was most likely triggered by emergence of oxygenic photosynthetic microorganisms
such as cyanobacteria. However, in spite of vigorous controversy
for decades since 1950’s, the timing of the oxidation event has not
been settled among scientists. Because billion-years-old “air bubbles” trapped in rocks have not been (and probably will not be)
discovered, we have to search for indirect evidence to constrain
the redox state of the ancient atmosphere and oceans. As such, we
mainly use geochemistry of sedimentary (and sometimes igneous)
rocks that formed during critical time interval, i.e., prior to 2.0 billion years ago.
This contribution aims to provide up-to-date listing of important literature for the discussion of “the timing of the rise of
atmospheric oxygen”, following a brief introduction of prebiotic
atmosphere and emergence of life. One of the IFREE’s main
objectives is to better understand how, when, and why anoxic
environments prevailed and how life responded, survived, and
evolved during the last 200 Ma. Connection of this contribution to
IFREE’s main objectives stems from attempts to understand
“anoxia” throughout the geologic history.
3. Emergence of life
The origin of life (i.e., timing and mechanisms) is not yet
known. It could be exogenous [delivery of extra-terrestrial organic
matter; e.g., Chyba et al., 1990; Chyba and Sagan, 1992; Chyba,
1993; Wallis and Wickramasinghe, 1995; Whittet, 1997] and/or
endogenous [hydrothermal / lightning synthesis of organic matter
on Earth; e.g., Miller, 1953; Miller and Urey, 1959; Farmer,
2000; Mancinelli and McKay, 1988; Navarro-González et al.,
2001]. The earliest emergence of liquid water on the Earth's surface is the crucial constraint on the timing of the emergence of
life, because liquid water is necessary for life's sustainability,
propagation and evolution.
A very early existence of the continental crust and oceans, as
old as 4.4 ~ 4.3 Ga ago, has been recently demonstrated [Wilde et
al., 2001; Mojzsis et al., 2001]. Therefore, life could have already
existed by ~4.4 Ga ago. Researchers have speculated that life may
have emerged rapidly, almost instantaneously in geologic
timescales, once the proper environment was provided on the
early Earth [Overbeck and Fogleman, 1989]. However, the very
early forms of life may have been almost completely destroyed by
the intense bombardments of planetary objects which continued
until ~3.8 Ga [e.g., Maher and Stevenson, 1988]. During that period, the early life could have repeatedly originated and then been
destroyed. Although some could have survived in niches, the earliest organisms are not necessarily the common ancestor of modern organisms.
The first form of life was probably not photosynthetic but
chemotrophic. In a pre-photosynthetic world, early microorganisms (probably chemotrophs) utilized local redox gradients to
obtain energy and nutrient elements such as Fe, P, Ni, and Mo
[e.g., Nisbet, 1995; Farmer, 2000] for life, probably near marine /
terrestrial hydrothermal systems.
2. Prebiotic atmosphere
The Earth's earliest, prebiotic atmosphere was essentially
devoid of molecular oxygen. After the main accretionary and
core-forming events occurred during the first few tens of millions
of years, the cooling of the Earth led to condensation of H2O
vapor and then the emergence of oceans. The residual atmosphere
was probably dominated by CO 2 , N 2 and H 2 O, with lesser
amounts of CO and H2 [e.g., Holland, 1984]. In the early atmosphere, UV radiation from the young Sun would have encouraged
photodissociation of H2O vapor, resulting in the loss of hydrogen
(to space) and accumulation of O2 in the atmosphere [e.g., Canuto
et al., 1983]. The UV radiation in the early atmosphere must have
been by far more intense than that of today [e.g., Canuto et al.,
1983]. However, O2 would have been consumed by oxidation of
reduced species in the atmospheric and the land/ocean surface and
by interaction with the mantle through volcanism (and subduction
if plate tectonics operated at that time) [e.g., Holland, 1984;
Kasting et al., 1993]. The accumulation of more than trace
amounts of O2 would depend on such an O2-sink. If the removal
of O2 by the reduced chemical species was rapid, as is likely due
to active tectonics and volcanics in the early Earth, the atmospher-
4. Source and sink of atmospheric O2
The most significant source of O2, photosynthesis, emerged on
the Earth by at least the Neoarchean [~2.7 Ga: Buick, 1992;
Beukes and Lowe, 1989; Brocks et al., 1999], and probably as old
as 3.5 Ga [Schopf and Packer, 1987; Awramik et al., 1983, 1988;
Schopf, 1993], possibly older than 3.8 Ga [Schidlowski, 1988,
2001; Mojzsis et al., 1996; Ohmoto, 1997; Rosing, 1999].
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FRONTIER RESEARCH ON EARTH EVOLUTION, VOL. 2
Oxygenic photosynthesizers, such as cyanobacteria, utilize the
light from the Sun to fuel growth and produce O2 as a by-product.
The overall chemical reaction of oxygenic photosynthesis is as
follows:
1.9 Ga. At face value, these observations appear to provide evidence for a reducing atmosphere prior to 2.2 Ga. However, a
detailed examination of each individual line of 'evidence' results
in, without difficulty, the realization that it is ambiguous and
maybe even misleading (Fig. 2). Such lines of controversial geological indicators for the rise of the pO2 level between 2.2 and 1.9
Ga are briefly summarized below and contrasted with alternative
interpretations. Detailed discussion on each topic listed below is
not the scope of this paper and therefore not presented. See
Holland [1994, 1999], Ohmoto [1997], and Phillips et al. [2001]
for more information. Also not presented in the compilation below
are studies that employ numerical calculations to predict redox
conditions of the early atmosphere [e.g., Kasting, 1987; Pavlov et
al., 2002] and those to predict the stability of oxic/anoxic atmosphere [e.g., Lasaga and Ohmoto, 2002].
CO2 + H2O → CH2O + O2
where "CH2O" represents organic matter. As a result of this
reaction, photosynthetic organisms started pumping O2 into the
atmosphere and began making the way for the later evolution of
multicellular life.
However, most of the O2 produced by oxygenic photosynthesizers was consumed by the backward reaction of the equation.
The O2 accumulation in the atmosphere becomes possible only
when the backward reaction of the equation is prevented; i.e., the
removal of CH2O from the system (the burial of organic matter in
the marine sediments). The burial flux of organic matter is equal
to the net O2 production flux into the atmosphere. However, the
atmospheric O2 budget reflects the balance between its net production by photosynthesis and its consumption by reduced volcanic gases and weathering [e.g., Holland, 1984, 2002; Berner
and Canfield, 1989].
6.1. Prevailing view: Low O2 before 2.2 Ga
The following geological observations have been used by
researchers to suggest that the pO2 levels were diminishingly low
before 2.2 Ga:
(1) Loss or retention of Fe in paleosols [e.g., Gay and Grandstaff,
1979; Grandstaff et al., 1986; Holland and Zbinden, 1988;
Zbinden et al., 1988; Holland and Beukes, 1990; Sutton and
Maynard, 1992; Macfarlane et al., 1994a, 1994b; Rye et al.,
1995; Rye and Holland, 1998; Pan and Stauffer, 2000;
Murakami et al., 2001; Yang and Holland, 2003];
(2) Mineralization mechanisms for the U ores [e.g., Davidson,
1953, 1957; Davidson and Cosgrave, 1955; Roscoe, 1973;
Minter, 1976, 1999; Grandstaff, 1980, 1986; Robertson, 1981;
Robinson and Spooner, 1982, 1984a, 1984b; Robb et al., 1992;
Robb and Meyer, 1995; Frimmel, 1997];
(3) Occurrence of O2-sensitive heavy minerals as detrital components in ~3 Ga sandstones [Rasmussen and Buick, 1999];
(4) Age-distribution of red beds [Cloud, 1968; Eriksson and
Cheney, 1992];
(5) Low content of redox-sensitive trace metals [e.g., Mo and U]
in black shales [Davy, 1983];
(6) Age distribution and formational mechanism of iron formations [e.g., Garrels et al., 1973; Beukes and Klein, 1992; Klein
and Beukes, 1989; 1992];
(7) Discovery of eukaryotes [Han and Runneger, 1992];
(8) Sulfur isotopic composition of sulfides and sulfates for the
secular changes in the S cycle [e.g., Cameron, 1982; Hattori et
al., 1983a, 1983b, Hattori et al., 1985; Cameron and Hattori,
1987; Canfield, 1998; Canfield and Raisewell, 1999; Habicht
et al., 2002];
(9) Mass-independent S isotope fractionation [Farquhar et al.,
2000, 2003; Bekker et al., 2004] [See also Ohmoto and
Yamaguchi, 2001; Deines, 2003; Yamaguchi, 2003b for criticism];
(10) Secular changes in the N cycle [Beaumont and Robert, 1999];
and
(11) Secular change of Th-U-Pb systematics of mantle [Collerson
and Kamber, 1999].
5. Controversy over the rise of atmospheric O2
The timing of the rise of O2 in the ancient atmosphere has been
vigorously debated since 1950, and no firm consensus has been
reached [Fig. 1; e.g., Berkner and Marshall, 1965; Cloud, 1968,
1972; Dimroth and Kimberley, 1976; Walker, 1977; Clemney and
Badham, 1982; Holland, 1984, 1994, 1999; Kasting, 1987, 1993,
2001; Lambert and Donnelly, 1991; Kasting et al., 1992;
DesMarais et al., 1992; Han and Runneger, 1992; Ohmoto et al.,
1993, 2001; Canfield and Teske, 1996; Karhu and Holland, 1996;
Ohmoto, 1996, 1997, 1999; DesMarais, 1997; Holland and Rye,
1997; Canfield, 1998; Rye and Holland, 1998; Beaumont and
Robert, 1999; Rasmussen and Buick, 1999; Canfield et al., 2000;
Farquhar et al., 2000; Kump et al. 2000; Catling et al., 2001;
Phillips et al., 2001; Lasaga and Ohmoto, 2002; Bekker et al.
2004; Huston and Logan, 2004; Ohmoto et al., 2004; Ohmoto and
Watanabe, 2004; Kasting and Sleep, 2004].
One school postulates a very low O2 level (10–13 to 10–3
PAL: present atmospheric level) before its dramatic rise to > 0.15
PAL between 2.2 ~ 1.9 Ga [GOE: Great Oxidation Event; e.g.,
Kasting, 1993; Holland, 1994, 1999, 2002]. In contrast, another
school postulates an essentially constant atmospheric O2 level
since at least 3.8 Ga [e.g., Dimroth and Kimberley, 1976; Ohmoto,
1997] (Fig. 1). As stated above, we must base any inference of the
history of the atmospheric O2 level on indirect evidence because
of the lack of a direct sample of the ancient atmosphere.
Geological records may have great potential to provide useful and
critical information concerning the redox state of the ancient
atmosphere. However, because of its indirect nature, much of it is
circumstantial and all of it is no better than semi-quantitative
[Holland, 1994].
6. Geological records bearing information on the
atmospheric O2
6.2. Emerging view: High O2 level since ~3.8 Ga
In contrast, the following lines of 'evidence' have been used by
researchers to suggest that pO2 levels were not so low in the early
Precambrian:
Figure 2 summarizes the lines of “geological evidence” to support the model of the rise of atmospheric O2 level between 2.2 ~
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FRONTIER RESEARCH ON EARTH EVOLUTION, VOL. 2
(1) Discovery of laterites at the top of a ~2.3 Ga paleosol profile
and its Fe isotope studies [Ohmoto et al., 1999; Beukes et al.,
2002, Yamaguchi et al., 2004a, 2004b, 2005a];
(2) Common occurrence of Fe loss in paleosol of all ages, including the Phanerozoic, caused by variable processes including
alteration by hydrothermal fluids, organic acids produced by
soil biota [Palmer et al., 1989; Ohmoto, 1996], and local factors such as climate / topography / groundwater filtration
[Schau and Henderson, 1983; Maynard, 1992];
(3) Development of oxidized paleosols of ~2.7 Ga in age [e.g.,
Kimberly and Grandstaff, 1986], of ~2.6 Ga in age [Watanabe
et al., 2000, 2004], of ~2.5 Ga in age [Nedachi Y. et al., 2004]
and of ~2.3 Ga in age [Panahi et al., 2000];
(4) Hydrothermal mineralization of uraninite and pyrite in U ores
[e.g., Phillips et al., 1987; Barnicoat et al., 1997; Nedachi M.
et al., 1998; Yamaguchi et al., 1998; Ohtake et al., 2004;
Yamaguchi and Ohmoto, 2005];
(5) Survival of detrital uraninite and pyrite in Phanerozoic sediments [Maynard et al., 1991; Maynard, 1992];
(6) Post-depositional mineralization (rather than detrital transport)
of siderite [Ohmoto, 1999];
(7) Discovery of 2.7 Ga old red beds [Shegelski, 1980];
(8) Occurrence of ferric oxide crust of pillow lava [Dimroth and
Lichtblau, 1978];
(9) Occurrence of iron-formations in Neoproterozoic [e.g., Klein
and Beukes, 1993] and Paleozoic [e.g., Peter, 2001];
(10) Geochemistry of banded iron-formations [Ohmoto et al.,
2005], especially for the presence of negative Ce anomaly
[Yamaguchi et al., 2000; Kato et al., 2005];
(11) Large variations in the S isotopic compositions of sulfides in
sediments [Ohmoto et al., 1993; Kakegawa and Ohmoto, 1999;
Kakegawa et al., 1999, 2000; Shen et al., 2001] and in volcanogenic massive sulfide deposits [Huston et al., 2001];
(12) Abundance of organic carbon in Archean shales suggesting
an operation of aerobic recycling [Towe, 1990, 1991, 1994;
Yamaguchi, 2002];
(13) Redox-sensitive trace elements (e.g., Mo and U) in black
shales [Yamaguchi and Ohmoto, 2001, 2002; Yamaguchi,
2002, 2003a, 2004d] and normal shales [Rosing et al., 2004];
(14) Discovery of biomarkers for cyanobacteria and eukaryotes in
Archean black shales [Brocks et al., 1999];
(15) Fe isotope compositions of black shales [Yamaguchi et al.,
2003, 2004c, 2004d, 2005a, 2005b]; and
(16) N isotope compositions of organic matter and clays in black
shales [Yamaguchi et al., 2002].
Researchers have drawn contrasting conclusions about the redox
state of the ancient atmosphere based on studies using similar sets
of samples (Fig. 2) and analytical methods. Such discrepancy
needs to be resolved toward formation of consensus among scientists on the timing of the rise of atmospheric oxygen. While much
more detailed geological and geochemical studies should be conducted in order to constrain the chemical evolution of the ancient
atmosphere, studies using relatively younger geologic materials
(such as those in Paleozoic and Mesozoic, or even those in
Cenozoic or modern sediments) and similar analytical methods
that are typically employed for Precambrian samples (e.g., 33S isotope analysis for Cenozoic rocks) are crucial and thus need to be
done. Such studies can be preferable targets of research at IFREE,
and likely to be useful to form a firm basis for correct interpretation of the geochemical and/or geological data for paleoenvironmental information hidden in the ancient rock records.
Acknowledgements. I thank Prof. Ohmoto for continued friendship and discussion on the topics presented above. Discussions with
members of IFREE4 and many other colleagues were also beneficial.
The initial draft of this paper was completed as a chapter of the Ph.D.
dissertation at The Pennsylvania State University [Yamaguchi, 2002],
and thus US National Science Foundation, NASA Ames Research
Center, NASA Exobiology Program, and NASA Astrobiology
Institute are appreciated for their generous financial supports.
Substantial revisions were made at IFREE for updates of the contents.
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Figure 1. Two contrasting models for the evolution of atmospheric O2 level. The "Constant O2 model" proposes the
emergence of cyanobacteria (oxygenic photosynthesizers) more than 3.8 Ga ago followed by a very rapid rise of
pO2 to the present atmospheric level. Nearly constant level of pO2 has been maintained since then. In contrast, the
"Evolutionary model" favors a dramatic rise of atmospheric pO2 level during 2.2-1.9 Ga (GOE: Great Oxidation
Event; Holland, 1999, 2002). PAL stands for "present atmospheric level".
Figure 2. Summary of controversial geological 'evidence' for pO2 in the early atmosphere. Vertical lines at 2.2 and
1.85 Ga bracket the proposed periods of sudden O2 rise (GOE: Great Oxidation Event) in the atmosphere (Holland,
1984, 1994, 1999, 2002). See text for more information. Modified after Holland (1994) and Phillips et al. (2001).
9