Available online at www.sciencedirect.

com

C. R. Palevol 8 (2009) 665–678

General palaeontology (Palaeobiochemistry)

Biological activity and the Earth’s surface evolution: Insights from

carbon, sulfur, nitrogen and iron stable isotopes in the rock record
Christophe Thomazo a,b,∗ , Daniele L. Pinti c , Vincent Busigny a,d , Magali Ader a ,
Ko Hashizume e , Pascal Philippot b
a CNRS UMR-7154, laboratoire de géochimie des isotopes stables, institut de physique du globe de Paris, université Paris 7, 75005 Paris, France
b CNRS UMR-7154, laboratoire de géobiosphère actuelle et primitive, IMPMC, institut de physique du globe de Paris, université Paris 7,

75005 Paris, France

c GEOTOP-UQAM, département des sciences de la terre et de l’atmosphère, université du Québec, QC, H2X 3Y7, Montréal, Canada
d CNRS UMR-7154, laboratoire de géochimie et cosmochimie, institut de physique du globe de Paris, université Paris 7, 75005 Paris, France
e Department of Earth & Space Sciences, Osaka University, 1–1 Machikaneyama, Toyonaka, Osaka 560-0043, Japan

Received 3 October 2008; accepted after revision 20 February 2009

Available online 5 August 2009

Written on invitation of the Editorial Board

Abstract
The search for early Earth biological activity is hindered by the scarcity of the rock record. The very few exposed sedimentary rocks
have all been affected by secondary processes such as metamorphism and weathering, which might have distorted morphological
microfossils and biogenic minerals beyond recognition and have altered organic matter to kerogen. The search for biological activity
in such rocks therefore relies entirely on chemical, molecular or isotopic indicators. A powerful tool used for this purpose is the
stable isotope signature of elements related to life (C, N, S, Fe). It provides key informations not only on the metabolic pathways
operating at the time of the sediment deposition, but more globally on the biogeochemical cycling of these elements and thus on the
Earth’s surface evolution. Here, we review the basis of stable isotope biogeochemistry for these isotopic systems. Rather than an
exhaustive approach, we address some examples to illustrate how they can be used as biosignatures of early life and as proxies for its
environment, while keeping in mind what their limitations are. We then focus on the covariations among these isotopic systems during
the Archean time period to show that they convey important information both on the evolution of the redox state of the terrestrial
surface reservoirs and on co-occurring ecosystems in the Archean. To cite this article: C. Thomazo et al., C. R. Palevol 8 (2009).
© 2009 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
Résumé
Apport des isotopes stables (C, N, S, Fe) à l’étude des interrelations entre activités biologiques et conditions physicochi-
miques de surface de la terre primitive. La recherche et la caractérisation des écosystèmes à la surface de la Terre primitive sont un
défi, étant donné le faible degré de préservation des roches archéennes. Les quelques formations sédimentaires disponibles ont, en
effet, été modifiées par de nombreux processus secondaires (métamorphisme, altération) qui excluent toute diagnose morphologique
robuste des microfossiles et des minéraux associés. La recherche de traces de vie fossile et la caractérisation des environnements
contemporains du dépôt reposent ainsi sur des indices chimiques dont les plus robustes sont les isotopes stables. Dans ce manuscrit,
nous tenterons de résumer les bases de la biogéochimie des isotopes stables et nous illustrerons comment cette discipline peut
permettre d’apporter des contraintes sur la vie primitive et son environnement. Quelques exemples choisis dans différents systèmes
isotopiques pertinents pour l’étude de la vie (C, N, S, Fe) et pour l’étude des conditions d’oxydation de surface de la Terre primitive

∗ Corresponding author.
E-mail address: [email protected] (C. Thomazo).

1631-0683/$ – see front matter © 2009 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.crpv.2009.02.003
666 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678

(fractionnement indépendant de la masse du soufre) nous permettrons d’illustrer de façon non exhaustive l’approche isotopique
et ses limitations dans la recherche de biosignatures. Enfin, nous présenterons les variations séculaires de ces 4 isotopes durant
l’Archéen, afin d’illustrer les interrelations biogéochimiques dans les cycles C-S-N-Fe. Pour citer cet article : C. Thomazo et al.,
C. R. Palevol 8 (2009).
© 2009 Académie des sciences. Publié par Elsevier Masson SAS. Tous droits réservés.

Keywords: Isotopes; Biosignature; Carbon; Nitrogen; Sulfur; Iron; Mass independent fractionation; Archean

Mots clés : Isotopes stables ; Biosignature ; Carbone ; Azote ; Soufre ; Fer ; Archéen

1. Introduction In the present contribution, we review four isotopic

system of biological interest (C, N, S, Fe). We develop
Life is maintained by a set of chemical reactions some examples for each, where we evaluate their poten-
called metabolism and organized into pathways, in which tial as a proxy for searching life. Finally, we review
one chemical compound (the reagent) is transformed the temporal isotopic variations of these four isotopic
into another (the product) by a sequence of enzymes. systems to illustrate the interplay of C-S-N-Fe biogeo-
Enzymes help living organisms to drive desirable but chemical cycling that occurred in ancient Earth.
thermodynamically unfavorable reactions by coupling
them to favorable ones. In most cases, for the same 2. Carbon isotopes
reaction (same reagents and same products), biotic and
abiotic pathways differ strongly in the mechanisms and 2.1. Biological fractionation of C isotopes
number of steps involved, and therefore in speed, yield
and – of particular interest here – in the fractionation of Carbon has two stable isotopes: 12 C accounting for
stable isotopes. 98.9% of the total abundance and 13 C, making up
Most of elements with stable isotopes show variations the balance of 1.1%. The international standard for
in the abundances of the minor relative to the major ␦13 C measurements is the PDB. Autotrophic organisms
isotope from one chemical species to the other. Their employ various pathways for inorganic C assimilation
partitioning between two chemical species A and B (i.e. carboxylation) with specific isotope fractionation
can be quantitatively described by a fractionation factor (see Table 1 ), which always favor the lighter isotope. The
(␣B/A = RB /RA ), where R represents the ratio between resulting Corg is thus 12 C-enriched relative to the inor-
the heavy and the light isotope. In general, isotope effects ganic C compounds from which it feeds from [83,85].
are small, ␣ ∼1, so that the deviation of ␣ from 1 is used In contrast, heterotrophic organisms have the same iso-
rather than the fractionation factor. For biologically topic composition as the organic matter they feed from.
mediated reactions, this quantity, to which we refer as the Thus, organic matter derived from heterotrophic organ-
fractionation, is defined by ␧B/A = 1000*ln(␣ B/A ) ≈ (␣ isms records the isotopic composition of the primary
producers in a food chain.
B/A –1)*1000. Practically, the isotope composition is
reported in the usual ␦-notation: ␦ = (R/RSTD -1)*1000, Fractionation during C assimilation is the result of
where R and RSTD are the sample and standard isotopic a kinetic isotope effect inherent to irreversible enzy-
ratios respectively. The fractionation can therefore be matic CO2 -fixing reactions. In case of the quantitatively
expressed simply as ␧B/A = ␦B – ␦A in parts per thousand. dominant carboxylation pathway by ribulose-1.5-
The validity of using stable isotopes of life-related bisphosphate (RuBP) carboxylase and the subsequent
elements (such as C, N, S or Fe) in the search for early Calvin–Benson cycle, the magnitude of the isotope effect
life hinges on the assumptions that early life employed mostly ranges between 17 and 30‰ (Table 1). This large
metabolic pathways essentially similar to those observed range derives from the facts that:
in the present and exerted similar fractionation effects. Its • the fractionation in enzymatic reactions varies widely
potential for identifying and characterizing metabolisms as a function of pH, metal cofactor, temperature and
in the rock record is illustrated by a rapidly growing number of other variables [129];
number of stable isotope studies on Archean sedimentary • the different types of RuBisCO enzyme are character-
rocks. It depends essentially on the difference between ized by different carbon isotope fractionation.
biotic and abiotic fractionation factors and the preserva-
tion in the rock record of pristine isotopic compositions RuBisCO IB and IA give a maximum fractiona-
of reagents and/or products of metabolisms. tion of ∼30‰ [111] and ∼24‰ [102], respectively
 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678 667

Table 1
Isotopic effect associated with the fixation of inorganic carbon by autotrophs. (Modified after [53]).
Tableau 1
Effet isotopique associé à la fixation de carbone inorganique par les autotrophes (modifié d’après [53]).
Carboxylation pathway ␧, ‰ Operated by

Calvin cycle/Rubisco (form I) 17–30 C3, C4 and CAM plants, algae

Calvin cycle/Rubisco (form II) 19.5–22 Cynobacteria, purple and chemoautotrohic bacteria
Reductive acetyl-CoA/methanogenese, acetogenese 15–58 Methanogenic bacteria (CO2 to CH4 )
Reductive acetyl-CoA 16–39 Sulfur reducing bacteria
3-hydroxyprorionate cycle 0–7 Anoxygenic photoautotrophic bacteria
Reductive citric acid cycle 4–13 Anoxygenic photoautotrophic bacteria

and RuBisco II has a smaller fractionation ∼19.5‰ associated to the recycling into biosphere and reminer-
in photoautotrophic purple bacteria [94]. Fractiona- alization in the water column and sediments. When the
tions are lower for anoxygenic photoautotrophic bacteria isotopic composition of the C source is recorded in the
that employ either the 3-hydroxypropionate pathway or ␦13 Ccarb , the difference between ␦13 Ccarb and ␦13 Corg
the reductive tricarboxylic acid cycle (Table 1; [106]). (13 Corg-carb = ␦13 Corg − ␦13 Ccarb ) can be used as a good
Anaerobes using the acetyl-CoA pathway can produce approximation of the kinetic effects associated to the
acetate and/or methane with a fractionation factor com- carbon assimilation pathways and can thus be used as a
prised between 15 and 58‰. Methane produced by proxy for life in sedimentary rocks.
methanogens bacteria using this pathway is probably
the most fractionated with extremely 13 C-depleted CH4 2.3. Fischer-Tropsch fractionation of C stable
relative to CO2 (∼58‰, [116]). Incorporation of this isotope
methane into biomass is performed during methan-
otrophic assimilation with an associated fractionation of The most important concern that could invalidate the
10 to 34‰ [131]. It produces the isotopically lightest use of C isotope as a proxy for life would be the existence
organic carbon observed in the terrestrial biosphere with of inorganic processes able to mimic, in direction and
␦13 C values < −80‰ [39]. magnitude, metabolic-induced isotopic fractionations.
One serious candidate is the Fischer-Tropsch Type reac-
tion (FTT), which produces reduced C from oxidized C
2.2. Identifying biological C isotope fractionation (e.g. CO2 ) in hydrothermal environments. Hydrothermal
in Archean rocks alteration of ultramafic rocks (serpentinization) leads to
the formation of H2 and minerals including serpentine,
Two distinct families of C-bearing compounds are magnetite and brucite. Produced H2 can reduce CO2 in
found in sedimentary rocks, namely organic carbon hydrothermal fluids to form CH4 and complex hydro-
(Corg ) and carbonate (Ccarb ). Carbonates are mainly com- carbons, including lipids [78]. A recent study has shown
posed of the skeletal remains of calcite or aragonite that hydrocarbons formed during FTT-synthesis have
secreting organisms, and of inorganically precipitated low ␦13 C (ca. −36‰ relative to CO2 -source), which is in
carbonate crystals in the water column, on the sea floor the range of most C isotopic signatures observed in Early
or as intergrain cements. In any case, carbonates record Archean rocks including those related to hydrothermal
the isotopic composition of Dissolved Inorganic Carbon precipitation of iron and silica [79]. Therefore, while
(DIC) from which they precipitate, with an offset of the C isotope signal is commonly used as a biosignature
the order of 1‰ due to thermodynamic isotopic equi- in sedimentary formation, it could be ambiguous in an
librium [82]. We can therefore use Archean ␦13 Ccarb Early Archean hydrothermal environment.
values as reliable indicators of the DIC isotope ratios
in early Earth environments, i.e., from surface waters 2.4. Post-depositional changes of the C isotope
to sediment porosity depending on the carbonate type. composition
Sedimentary organic matter originates from residues
of living organisms, which have survived remineraliza- In metamorphosed Archean sedimentary rocks, ther-
tion. Several parameters control its ␦13 Corg ([123] for mal devolatilization of organic matter (production of
a review), including source effects (isotopic composi- CH4 and CO2 ) and isotopic exchange between organic
tion of the DIC), kinetic effects associated to the C C and carbonates may have modified the initial ␦13 Corg .
assimilation and to a minor extend, the kinetic effects Devolatilization processes can shift C isotope composi-
668 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678

tion of the residual carbonaceous matter towards higher isotopic exchange between these two phases may occur
values due to preferential loss of 12 C. The isotopic shift and decreases the isotope difference between Ccarb and
is usually estimated from a relation between ␦13 Corg and Corg with increasing temperature [119]. The 3.8 Ga
H/C ratio [36,54]. However, in some cases, no isotopic sedimentary rocks of Isua Supracrustal belt (Southwest
shift is observed (see for example [101]) and corrections Greenland) offer a good example of extremely ambigu-
should be carefully employed. When both carbonate ous ␦13 Corg data in metamorphosed rocks. These rocks
and organic C co-exist in a rock, metamorphic-driven experienced amphibolite facies metamorphism (500 ◦ C;

Fig. 1. Secular variations of C (kerogens and carbonates), N (kerogens, micas and bulk shales, cherts and BIF), S (sulfides, sulfate and barite) and Fe
(sulfides, Fe oxides from BIF, carbonates, bulk shales and BIF) isotopic compositions through the Archean and Late Proterozoïc eon (3.8 to 2.0 Ga).
The gray field underlines transient and extensive variation of C, N, S and Fe isotopic composition around 2.7 Ga. Mass independent fractionation of
sulfur is expressed using the conventional 33 S, and the blue field refers to mass dependent range of 33 S. Data of the compilation and references
are provided in a separate table as supplementary material.
Fig. 1. Variations séculaires des compositions isotopiques du C (kerogènes et carbonates), de l’N (kerogènes, micas, shales, cherts et BIF), du S
(sulfures, sulfate et barite) et du Fe (sulfures, oxydes de Fe extraits de BIF, carbonates, shales et BIF), au cours de l’Archéen et du Paléoprotérozoïque
(3,8 à 2,0 Ga). La zone grisée souligne une excursion des compositions isotopiques du C, N, S et Fe autour de 2,7 Ga. Le fractionnement indépendant
de la masse du soufre est exprimé en utilisant la notation 33 S et la zone bleue représente la gamme de variation du 33 S masse dépendante. Les
données compilées et les références sont fournies sur un tableau séparé en tant que document supplémentaire.
 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678 669

3–5 kbar), so that their carbonaceous matter is present 3.1. N isotopes fractionation in biological systems
as graphite. In metacarbonates, bulk carbonate and
graphite carbon isotope compositions range from −12 The first step in N cycling is biological fixation of
to −10‰ and −9 to +1‰, respectively. The low values atmospheric N2 by aerobic or anaerobic autothrophs,
and the variability of the isotope fractionations between such as cyanobacteria, which have the nitrogenase
graphite and carbonate, are more compatible with var- enzyme that combines gaseous N with hydrogen to pro-
ious extent of isotopic exchange during metamorphism duce ammonia (NH3 ) with little isotopic fractionation
than with values inherited from the deposition time (␧ ≤ 2‰; [105]). Ammonia is quickly assimilated and
[118]. However, graphite globules armored in garnet incorporated into proteins and other organic N com-
crystals present lower ␦13 C values of ∼ −19‰ [95]. pounds, through the process of uptake. Organic-N is
The garnets being supposed to have sheltered to some often converted back into inorganic N by mineraliza-
extent the graphite from isotope exchange, their ␦13 C tion. This process produces an enzymatic breakdown of
values are the closest known so far to the initial organic organic matter to release amine groups (-NH2 ) of amino
matter ␦13 C, which must have been lower and thus acids and subsequently NH4 + through ammonification
arguably of biological origin. with little isotopic fractionation (␧ ≤ −5 to +0‰; [105]).
Under aerobic conditions, NH4 + is rapidly oxidized to
2.5. The isotope record of a life operated C cycle in nitrite (NO2 − ) and subsequently to nitrate (NO3 − ) in
the Archean a two-step process called nitrification, where a strong
isotopic fractionation is produced (␧ = −17‰; [105]).
A systematic difference in the isotope composi- Marine organisms can recycle nitrates by:
tion of organic and carbonate C reservoirs (Fig. 1)
– with 13 Corg-carb ∼ −30‰ – has been observed in • nitrate uptake or assimilation with a relatively cons-
most organic-rich sediments of different ages from 3.5 tant ␧ of +5‰ [105];
to 2.0 Ga (Fig. 1). This carbon isotope record is an • in suboxic environments, nitrate is stepwise reduced
important, uninterrupted evidence for the presence of to gaseous N2 by heterotrophic bacteria that can use
a substantial biosphere over geological time down to NO3 − as alternative electron acceptor when O2 is not
∼3.5 Ga [54,99]. The ␦13 Corg record shows a nega- readily available.
tive excursion between ∼2.7 and 2.6 Ga (Fig. 1), with
␦13 C values as low as −60‰, while carbonate ␦13 C This process, called denitrification is characterized by
values remain close to 0‰ [35,52,113]. This transitory a much larger isotope effect (␧ = −25‰) [105], which is
13 Corg-carb ∼ −60‰ suggests that methanotrophy, and responsible for the enrichment in 15 N of oceanic nitrate
hence methanogenesis, was contributing significantly to (relative to atmospheric N).
the C cycling during this period. The ␦15 N of nitrate resulting from this multistep
kinetic metabolic fractionation is ∼ +5‰ [105]. Because
3. Nitrogen isotopes nitrate is utilized by primary producers, the ␦15 N of the
sinking flux (and of organic matter prior to diagenesis)
Nitrogen – a common element in proteins and nucleic will be close to 5‰ [88]. Diagenesis should have little
acids – has two stable isotopes: 14 N (99.6337%) and 15 N isotopic effect on the N of fixed ammonium as disclosed
(0.3663%) [103]. The international standard for ␦15 N by the isotopic similarity of oceanic Norg (␦15 N = +5‰)
measurements is Air. Nitrogen mainly occurs in rocks with the bulk sedimentary N (␦15 N = +7 ± 1‰)
as organic nitrogen in the carbonaceous matter and fixed [3,88].
ammonium (NH4 + ), derived from the decomposition of
organic molecules during diagenesis and early stages of 3.2. The Archean biogeochemical cycling of
metamorphism. Fixed NH4 + is firmly bound in the lat- nitrogen
tice structure of K-bearing minerals, where it can replace
K+ ions [10,56]. The ␦15 N value of fixed NH4 + can be Beaumont and Robert [8] showed an evolution of
considered as a relatively good proxy of the isotopic the N isotopic signature of kerogens with ␦15 Nkerogen
composition of organic N [100,128], the isotope effect from −6.2‰ in the Early Archean to +10‰ in the
associated with diagenesis being usually smaller than a Late Proterozoic. This evolution was interpreted as
few per mill [97]. The ␦15 N in modern marine bulk sedi- changes in the redox potential of the Earth towards
ments is indeed of +7 ± 1‰ [88], close to that measured more oxidizing condition around the Great Oxidation
in the oceanic organic matter influx +5‰ [3]. Event [55]. The increase of atmospheric O2 at the end
670 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678

of the Archean would have encouraged the biological than heavier) primeval N inherited from prototerrestrial
production of NO3 − and its use as a source for organic material [114].
15 N-enriched nitrogen.

Earlier negative ␦15 N values during Archean might 3.3. N secular variations, redox conditions and the
reflect a metabolic isotopic fractionation in anoxic condi- emergency of metabolisms
tions, when the oceanic nitrate pool was scarce. Bacteria
might have used reduced, inorganic forms of nitro- In Fig. 1, we reported all published (and unpublished
gen through NH4 + uptake [43] and NH3 assimilation data from D. Pinti internal database) N isotopic data
[7], which are able to produce some negative isotopic measured in bulk rocks and kerogens, plotted against
shift. Alternatively, Beaumont and Robert [8] argued that time since Earth formation. Paleoarchean (3.8–3.2 Ga)
atmospheric N2 could have been isotopically lighter than N isotopic signatures exhibit a bimodal distribution,
today (␦15 N = −5‰) if derived from an Enstatite Chon- with ␦15 N values from −7 to +7‰ [92]. Nitrogen from
drite source [60] and thus, simple biological fixation of Neoarchean organic matter (3.2–2.5 Ga) is much more
that N could have been reflected in the organic pool. 15 N-enriched, with a ␦15 N
mean value around +11‰.
Pinti and Hashizume [90] and Pinti et al. [91] chal- In a restricted range of age clustered around 2.7 Ga,
lenged the interpretation of Beaumont and Robert [8], kerogens, cherts and particularly BIF show an extreme
suggesting that their kerogens represented an envi- enrichment in 15 N (from +24‰ up to +35‰; [8,62]).
ronmentally biased sample of the Archean biota, in Proterozoic kerogens and cherts show lower ␦15 N, with
that many were extracted from silica precipitated from an average of +5.6‰, close to the value of modern ocean
hydrothermal fluids. In such anoxic setting, metabolic nitrates. It is worth noting that the large positive shift
processes are regulated by chemosynthetic biota [26]. in the N isotopic composition measured in kerogens
Chemoautolithotrophy describes the synthesis of organic and rocks is reached before the Great Oxidation Event
C compounds from CO2 using energy and reduc- (2.35 Ga; [9]), during the largest deposition of Banded
ing power derived from the oxidation of inorganic Iron Formation (BIF) ever on Earth, between 2.7 and
compounds, such as NH4 + , which support microbial 2.6 Ga [58]. The deposition of BIF requires the presence
chemosynthesis [59]. The N isotopic signature of the of little oxygen, possibly 10-2 Present Atmospheric
biomass produced by chemosynthesis, via N fixation Level (PAL) or less [57]. If these conditions were
[70,80] is significantly depleted in 15 N, with ␦15 N values sufficient to have limited the amount of nitrates in the
ranging from −9.6 to +0.9‰ [25,26,70,86,117]. ocean, we could speculate that the observed elevated
N isotopic ratios measured in Late Archean (2.7 Ga) ␦15 N values were obtained by enhanced denitrification
shales and kerogens by Jia and Kerrich [62,63] and Ker- [2,3]. The degree of N kinetic isotope fractionation
rich et al. [71] showed exclusively positive ␦15 N values depends on the nitrate availability as a reactant: the
from +5 to +24‰. They interpreted the high ␦15 N val- lower the reactant availability, the higher the isotopic
ues as a fossil residual signature of a veneer atmosphere effect that can be produced by Rayleigh distillation
having an initial CI-chondritic composition with ␦15 N [105]. In a nitrate-poor Archean ocean, the nitrification-
values from +30 to +42‰. The isotopic shift from +24 denitrification-assimilation processes could have easily
at 2.7 Ga to 0‰ at present was interpreted as the combi- produced a higher nitrate ␦15 N than in the modern
nation of three processes: ocean. With the increase in oceanic nitrate content
following the oxygenation of the ocean at the end of
• degassing of 15 N-depleted mantle N
Archean, the nitrate isotopic composition would have
(␦ N = −5 ± 2‰);
15
decreased to the modern average value of +5‰.
• progressive sequestration of atmospheric chondritic-
like N in sedimentary rocks by fixing organisms;
3.4. Limits in the use of N isotopes as a reliable
• return flux of 15 N-depleted nitrogen to the atmosphere
biotic signature
as a byproduct of some sort of metabolism.
However, the occurrence of an isotopically heavier Post-depositional changes of the pristine, metabolic-
atmosphere during Archean can be dismissed by the induced N isotopic fractionation are difficult to evaluate.
presence of very variable negative ␦15 N values in Studies on thermal metamorphism showed that the
Archean diamonds from −5 to −10‰ and down to ␦15 NNH4 + measured in mica increased progressively
−25‰ [22] which possibly reflect the mixing of a with the metamorphic grade up to +15‰. This isotope
crustal component and an atmospheric component shift was interpreted as a progressive devolatilization of
recycled into the mantle with isotopically lighter (rather the rock (with preferential loss of lighter 14 N compared
 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678 671

to 15 N) by increasing temperature [49]. Dauphas and • disproportionating metabolisms which obtain energy
Marty [30] showed that devolatilization could have from the hydrolysis of elemental S, thiosulfates or
caused large isotopic shift (≥ 15‰) in some Archean sulfites.
hydrothermal mica. However, recent studies have shown
that during regional metamorphism (high pressure, We describe below the S isotope fractionations associ-
high temperature) the ␦15 NNH4 + shift is limited to ated with these three processes. The fractionation (␧34 )
+2 − 3‰ (e.g., [14,61]), while the ␦15 Nkerogen shift is imposed by BSR between initial sulfate and produced
null [1]. Moreover, as for carbon, the most important sulfides varies from 4 to 46‰ [23,50,68]. It depends on:
concern that could invalidate the use of N isotopes as
biosignature would be abiotic processes mimicking • the organism involved [34];
metabolic-induced isotopic fractionations. The few • the sulfate concentration [17,48];
experimental data existing on N isotopic fractionation • the sulfate reduction rates [16,34,47].
during FTT synthesis of N-based polymers and amino
acids gave contradictory results. Miller–Urey reactions At high sulfate concentrations, the biological sulfur
of CH4 –NH3 –H2 mixtures have produced N-containing isotope fractionation of natural populations of sulfate
nonvolatile soluble organics (amino acids, organic acids) reducers is typically comprised between 20 and 40‰,
and polymers with ␦15 N values 8 to 11‰ greater than independently of temperature and reduction rate [16,46].
the starting NH3 [75]. Plasma-discharge of CO–N2 –H2 At low sulfate concentrations (less than 200 ␮M), it is
produced carbonaceous materials with ␦15 N values of greatly reduced [16,50].
−3 to −17‰ relative to the reactant N2 [72]. These The biological pathways of sulfides oxidation in
few experimental evidences do not allow estimating nature are diverse and poorly known. They include
whether FTT reactions could have an important role in phototrophic and non-phototrophic oxidation of various
N isotopic fractionation in Precambrian rocks. sulfide species such as H2 S, S0 , S2 O3 2− and SO3 2− .
The fractionations produced during phototrophic oxi-
4. Sulfur isotopes dation are small or negligible (between −2 and 0‰
[41,42]). Small fractionation also accompanies the non-
Sulfur has four stable isotopes 32, 33, 34 and 36. The phototrophic oxidation between −1 and 1‰ [68].
most abundant is 32 S, representing ∼ 95% of the total sul- Three different disproportionation reactions involv-
fur on Earth. The 34 S contributes to 4.22%, 33 S to 0.76% ing intermediate S compounds are known: S0 (4S0
and 36 S contributes only to 0.0136% of the total [103]. + 4H2 O → 3H2 S+ + SO4 2− + 2H+ ), S2 O3 2− (S2 O3
2− + H O → H S + SO 2- ), and SO 2- (4SO 2− + 2H+
The international standard for ␦34 S and ␦33 S measure- 2 2 4 3 3
ments is V-CDT. Sulfur has a wide range of redox states, → H2 S + 3SO4 2− ). The fractionation associated with
spanning from oxidized sulfate (SO4 2- : +VI) to reduced the disproportionation of elemental S shows a narrow
hydrogen sulfide (H2 S: -II). This range of redox states range, where sulfide is depleted in 34 S by 6.1 ± 0.4‰,
promotes cycling in surface environments and catalyzes and sulfate is enriched in 34 S by 18.3 ± 1.3‰ [21].
34 S depletions higher than 70‰ recorded in natural
the production of a large range of isotopic fractionations
from – 60 to +130‰ in ␦34 S [27]. sulfides derive from multistep sulfide oxidation of sulfur
intermediate subsequently disproportionated, and so
4.1. Biological sulfur isotopic fractionations on [20]. Inorganic disproportionation involves only a
minor < 3‰ kinetic isotope fractionation [108].
The Earth surface cycle of S is dominated by biolog-
ical processes, which utilize the eight-electron S redox 4.2. Abiotic sulfur isotopic fractionations
gradient and impart large S isotopic fractionations.
Organisms generally use S according to three main High temperature hydrothermal processes (> 100 ◦ C)
processes: promote the abiological thermo sulphate reduction
(TSR) to sulfides [44]. The maximum isotopic frac-
• bacterial sulfate reduction (BSR), where sulfate acts tionation associated to TSR is ∼20‰ at 100 ◦ C.
as an electron acceptor during organic C oxidation (i.e. Therefore, while the S isotope signal is commonly used
respiration) or H2 oxidation; as a biosignature of BSR and disproportionation in
• sulfides oxidation, where sulfides species act as an sedimentary formations, it could be ambiguous in Early
electron donor associated to O2 , NO3 − or CO2 reduc- Archean hydrothermal formations [77]. Sulfides could
tion; also derive from H2 S released from NSO-compounds,
672 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678

with kinetic sulfur isotope fractionation lower than and sulfates have provided new insights into the
−2‰ [77]. Hence, sulfides produced by organic matter Archean sulfur metabolisms and oxygenation his-
thermal cracking should present much heavier ␦34 S tory. The multiple S isotope studies revealed S
values than those formed by BSR. anomalous mass-independent fractionation (MIF-S)
[9,37,81,87]. MIF-S is expressed by the 33 S (i.e.
4.3. Identifying biological sulfur isotope 33 S = ␦33 S-1000*[1 + ␦34 S/1000]0.515 − 1) and refers
fractionation in the rock record to any chemical or physical process that acts to sepa-
rate isotopes, where the amount of separation does not
Sulfur isotope measurements are performed essen- scale in proportion with the difference in the masses of
tially on three families of sulfur-bearing compounds the isotopes (see review in [112]). Most isotopic frac-
which can be found in the rock record. Evap- tionations (including typical kinetic fractionations and
orite sulfate minerals (gypsum, anhydrite, barite), equilibrium fractionations) are mass dependent since
carbonate-associated sulfates (CAS) and sulfur miner- they are caused by the effects of the mass of an isotope
als (essentially pyrite). Both evaporites and CAS record on atomic or molecular velocities, diffusivities or bond
faithfully the isotopic composition of the dissolved sul- strengths. MIF processes are less common, and for sulfur
fate they originate from, and pyrite precipitates from isotopes are known to occur during UV photolysis of SO2
dissolved sulfide with a small isotope fractionation and SO. In its most basic form, photolysis produces two
(∼1‰, [93]). Thus, the difference between sedimentary isotopically-distinct types of sulfur bearing aerosols that
sulfate (evaporite or CAS) and pyrite isotope com- are likely to rain out to Earth’s surface environments and
positions can be used as an indicator of BSR and S transfer positive 33 S via reduced sulfur species (S0 ) and
disproportionation pathways. negative 33 S via oxidized sulfur species (H2 SO4 ) to the
Between 3.5 and 2.4 Ga, sulfate ␦34 S secular evolu- sedimentary record. MIF-S are thought to be produced
tion seems to be centered on 0‰. It is however poorly and preserved in the sediments only when atmospheric
constrained so far because of the lack of evaporite sul- partial pressure of O2 is lower than 10-5 PAL, thus
fates minerals in the rock record, and the scarcity of preventing both oxygen UV shielding effect and re-
available ␦34 S data on CAS (Fig. 1). Pyrite ␦34 S Archean homogenization of atmospheric sulfur species through
secular evolution is better constrained and is also cen- oxidation [38,69,98]. MIF-S are significant (i.e. different
tered around 0‰, except for the Dresser Formation from 0‰) from 3.8 to 2.4 Ga (Fig. 1) and therefore, pro-
(western Australia) at ∼3.49 Ga, where ␦34 Spyrite are vide evidence for a low atmospheric O2 content before
lower than −20‰ (Fig. 1) and interpreted as a biolog- 2.4 Ga [9], and for a very different atmospheric S chem-
ical signature in spite of the fact that they belong to a istry in the Archean. Moreover, the sign of 33 S can
hydrothermal system [89,104] (see § 5.4). The range be used to trace the oxidation state of the source of the
of ␦34 Spyrite around 0 ± 5‰ observed in most Archean sedimentary S component. This approach was recently
pyrites can thus be interpreted either as an absence of evi- used to re-evaluate the significance of the strongly nega-
dence for the operation of BSR/disproportionation [109], tive ␦34 Spyrite observed in the 3.49 Ga Dresser Formation
or, assuming that these sulfur metabolisms were operat- (Pilbara, western Australia), which was suggested to
ing [46,104], as the evidence for a sulfate-poor ocean reflect the first evidence of BSR in a locally sulphate-rich
[17]. At ∼2.4 Ga, the increasing range of ␦34 Spyrite pro- Early Archean environment [104]. Combined observa-
vides indisputable evidences both for the involvement of tion of negative ␦34 S and positive 33 S of sulfides was
BSR and/or disproportionation in the sulfur cycling and interpreted as evidence for reduced S conversion to sul-
for an increasing ocean sulfate concentration. Assum- fides by S disproportionating microorganisms [89].
ing that the sulfate concentration in the oceans depends
on the rate of pyrite oxidative weathering [18,110], 5. Fe isotopes
this increase in sulfate concentration is interpreted as a
response to a rise in the atmospheric O2 content known 5.1. Fe isotopes fractionation in biological systems
as the Great Oxidation Event (see [55] for a review).
Iron has four stable isotopes, 54 Fe, 56 Fe, 57 Fe and
58 Fe,with natural abundances of 5.84, 91.75, 2.12 and
4.4. Combined multiple sulfur isotope study: a
window to Archean sulfur metabolisms 0.28%, respectively. The isotope ratio 56 Fe/54 Fe used
by most authors is expressed as ␦56 Fe, referred to
More recently, combined isotopic measurements the IRMM-014 standard. The most important param-
of ␦33 S, ␦34 S and ␦36 S from Archean sulfides eters controlling Fe isotope fractionations in natural
 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678 673

environment are oxidation state and bonding. In aqueous Fe(III) substrates and bacterial species [28]. Bacterially-
system, ferric iron (Fe[III]) is soluble under acidic and mediated Fe dissolution is thus associated with large
oxidizing conditions but is insoluble under near neutral- isotope fractionation. Abiotic dissolution of minerals
pH conditions. Ferrous iron (Fe[II]) is soluble over a seems to be more complex. Some experiments as well as
large range of pH under anoxic conditions. Cycling of natural environment study illustrate that abiotic dissolu-
Fe is not only controlled by Eh-pH conditions but also tion of minerals did not produce significant Fe isotope
by living organisms that derive energy through changes fractionation [11,12,15,107]. Abiotic goethite dissolu-
in Fe redox state [76,84]. Organisms generally use Fe tion shows different results depending on the mechanism
according to three main processes: of dissolution. Proton-promoted dissolution produces no
fractionation, while ligand-controlled and reductive dis-
• Fe(II) oxidation, where Fe(II) acts as an electron donor solution enrich the produced Fe(II)aq in the light isotopes
for energy generation; by 1.7‰ relative to reactive surface [126]. These abi-
• dissimilatory iron reduction (DIR), where Fe(III) acts otic fractionations were significant for the first steps
as an electron acceptor for respiration; of substrate dissolution but were negligible after only
• assimilatory Fe metabolism, where Fe is incorporated ∼2% of the initial substrate dissolved. Accordingly, abi-
into biomolecules. otic mineral dissolution produces either no or limited
fractionation of Fe isotopes. While the direction of the
We describe below Fe isotope fractionation associ- fractionation is the same for biotic and abiotic dissolu-
ated with these three processes. tion, the amplitude is much larger (by at least ∼1‰) in
The oxidation of Fe(II) under anoxic condition the case of microbial dissolution. When microorganisms
can be performed by phototrophic or chemotrophic have intense metabolic activity, they can produce a large
metabolisms. Fe(II) can also be oxidized indirectly by amount of Fe(II)aq with very light Fe isotope signature
microorganisms when reacting with O2 released from under conditions out of equilibrium.
oxygenic photosynthesis. The oxidation of Fe(II)aq into Iron assimilation in microorganisms is largely due to
Fe(III)aq leads to insoluble species such as Fe oxihydrox- the two stable valencies that impart considerable range
ide that evolve ultimately into goethite, hematite and/or to the reactivity of Fe. When inserted into organic ligand,
magnetite. Isotopic studies of Fe oxides and hydroxides Fe can be used to catalyze a wide range of chemi-
stored in sedimentary rocks may thus reveal the signature cal reactions essential to the cell. Fe is also the active
of life. Unfortunately, experimental works showed that component of the O2 carrier proteins. Only few studies
the oxidation of Fe(II)aq to Fe(III)aq enriches Fe(III)aq have examined Fe isotope fractionation during uptake by
in the heavy isotopes by ∼1 to 3.4‰, regardless on microorganisms [11,12,121]. Experimental work indi-
whether this oxidation is biologically mediated or not cates that bacterial Fe assimilation favors uptake of
[4,5,64,122]. The enrichment in heavy Fe isotopes dur- heavy isotope into the cell, with a fractionation of
ing oxidation is usually counterbalanced by a kinetic ∼1.1‰ [121]. This fractionation cannot be explained by
isotope fractionation during precipitation, enriching the a simple kinetic process (since lighter isotopes should be
precipitate in the light isotopes [107]. Overall, the net favored) and requires at least one step in isotopic equi-
isotopic fractionation is modulated by the rate of pre- librium. However, whether it reflects active microbial
cipitation but, in most cases, it produces a precipitate assimilation or passive adsorption of Fe on cell walls is
enriched in the heavy isotopes of Fe. still unknown.
Bacterial DIR is a widespread process in anaero-
bic marine sediments and may be one of the oldest 5.2. The Archean biogeochemical cycling of iron
forms of respiration [120]. This process couples the
oxidation of organic matter to the reduction of solid The earliest photosynthetic metabolism on Earth
Fe(III). In addition to the production of Fe(II)aq , the end- was probably anoxigenic. Because Fe(II) was the most
products of DIR may include Fe carbonates (siderite important electron donor available in the Archean ocean,
and ankerite) and magnetite [76]. Microbial DIR pro- anaerobic Fe(II) oxidation may have been the main
duces Fe isotope fractionation enriching Fe(II)aq in the metabolic pathway [19,125]. This biogenic oxidation of
light isotopes relative to the initial Fe(III) substrate Fe(II)aq into Fe(III)aq produces insoluble Fe oxihydrox-
[6,12,28,65]. In experiments of bacterial DIR, the Fe ide and is often considered to explain the deposition of
isotope fractionation between Fe(II)aq and a reactive BIF in the Archean [51,73]. Other hypotheses to explain
Fe(III) component on a Fe(III) oxide surface was found the formation of BIF include Fe(II) oxidation through
constant at −2.95‰ over long timescales, for various increase in ambient O2 by photosynthetic activity [24]
674 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678

and abiotic Fe photo-oxidation by UV photons [13]. As metamorphic disturbance, which should produce iso-
noted above, Fe isotopes alone cannot differentiate biotic topic homogeneization. In contrast, Fe isotope hetero-
from abiotic oxidation. However, a recent study coupling geneity likely derives from isotopic reservoir effect
laboratory experiments with thermodynamic modeling during diagenetic reactions in pore waters isolated from
seems to rule out the possibility of a photo-oxidation the ocean [124]. In Biwabik Iron Formation, Fe isotope
[74]. If this is true, the two other scenarios involve living fractionation between coexisting minerals decreases
organisms, either as oxygenic or anoxygenic photosyn- with increasing metamorphic grade, indicating that iso-
thetic metabolism. topic exchange occurred during metamorphism [115].
Before deciphering biogeochemical index of life from Isotopic exchange was limited to the mineral-scale but
Fe isotopes, it is crucial to understand the cycling of Fe bulk rock behaved as closed-system and preserved pri-
in the Archean. Large variations in the Fe isotope record mary Fe isotope composition [40,115]. Any potential
were identified during Archean and Early Proterozoic isotopic re-equilibration could be avoided by analyzing
by analyzing sedimentary pyrites [96]. Fig. 1 plots a metamorphic rocks or layers with single Fe-bearing min-
compilation of Fe isotope data available in the litera- eralogy, which may be particularly useful for searching
ture for Archean rocks. The most significant variation isotopic traces of early life.
is a large negative excursion of ␦56 Fe values between
2.7 and 2.3 Ga flanked by near zero or slightly pos- 6. Conclusion
itive ␦56 Fe values before 2.7 Ga and after 2.3 Ga. It
was primarily interpreted as reflecting changes in the Major changes of C, N, S and Fe isotopic composi-
Fe isotopes signature of seawater [29,96]. However, this tions are recorded between ∼2.8 and ∼2.5 Ga (Fig. 1)
interpretation is weakened by the observation of large Fe and can be interpreted in terms of environmental and
isotope heterogeneity (> 2‰) at the cm-scale in Archean associated-metabolic changes. The ␦13 C measured in
rocks, which cannot be explained by secular variation organic matter shows a large negative isotopic shift from
in seawater, because of the high Fe residence time in −30‰ down to −60‰ and back to −30‰, while ␦56 Fe
the Archean ocean [65]. Although such a small scale values, which are mainly around 0‰ over the last 4 Ga
variability has only been reported once and still needs show in this particular period a decrease down to −4‰
some confirmation, an alternate hypothesis has been pro- (Fig. 1). MIF-S show variations from −0.5 to +1.4‰
posed which is that the ␦56 Fe of sedimentary rocks might between 3.2 and 2.8 Ga, and a larger range, from −2.5
reflect mainly biogeochemical cycling during sediment to +11.2‰, between 2.7 and 2.45 Ga before disappear-
diagenesis [66,67,130]. The large negative excursion of ing after 2.4 Ga [9]. Negative ␦34 S values < −17‰ are
␦56 Fe values between 2.7 and 2.3 Ga would result from also recorded at 2.7 Ga in the Belingwe belt (Zimbabwe)
an extensive activity of DIR metabolism in response [45]. Finally, the ␦15 N shows an extreme enrichment in
to increase Fe(III) and organic carbon delivery to the 15 N (from +24 up to +35‰; [8,62]) around 2.7 Ga com-

ocean [65]. If true, this exciting alternative would indi- pared to Paleoarchean ␦15 N (between −7 and +7‰ [92])
cate that Fe isotopes do record the signature of iron based and Proterozoic ␦15 N (average of +5.6‰).
metabolic pathways. The isotopic covariations around 2.7 Ga are probably
related to a change of the ocean redox conditions [65]
5.3. Limits in the use of Fe isotopes in Archean rocks and point to the development of metabolisms using oxi-
dized species in the oceans. Low ␦13 Corg and ␦34 Spyrite
The drawback with studying old Precambrian rocks observed in the Belingwe belt (Zimbabwe) and in the
is that most of them experienced metamorphism. Tumbiana Formation (western Australia) suggest that,
An important question is thus whether Fe isotope at least locally, sulfate concentration was high enough
composition reflects processes in water column, sedi- to support anaerobic oxidation of methane and BSR
ment diagenesis or metamorphism. Several works on [45,113]. The same conclusion in favor of a more oxidiz-
Eoarchean metamorphic rocks demonstrated that Fe iso- ing oceanic environment arises from N and Fe isotopic
topes can be used to distinguish protolith signature variations that may reflect the use of a limited pool of
from metamorphic overprint [31–33]. Whitehouse and nitrates for nitrification-denitrification processes and the
Fedo [124] observed small-scale isotopic heterogene- use of Fe(III) by DIR activity [67], respectively. Ris-
ity in magnetite from very small areas within single ing of oxidant in the ocean at around 2.65 to 2.5 Ga is
bands of Eoarchean BIF, indicating a range of fraction- also supported by recent development of Mo isotopic
ation within single depositional event. This is unlikely study [127]. Despite indication of oceanic oxygena-
to have resulted from water column chemistry or later tion, significant 33 S around 2.7 Ga suggests that the
 C. Thomazo et al. / C. R. Palevol 8 (2009) 665–678 675

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Appendix A. Supplementary data recycling of nitrogen and other fluid-mobile elements (K, Rb,
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Supplementary data associated with this article can oceanic metasediments of the Schistes Lustrés nappe (western
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