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228
ISSN 0031-0301, Paleontological Journal, 2019, Vol. 53, No. 3, pp. 228–240. © Pleiades Publishing, Ltd., 2019.
Russian Text © The Author(s), 2019, published in Paleontologicheskii Zhurnal, 2019, No. 3, pp. 15–26.
Archean Fossil Microorganisms
M. M. Astafieva*
Borissiak Paleontological Institute, Russian Academy of Sciences, Moscow, 117647 Russia
*e-mail: astafieva@paleo.ru
Received March 30, 2018; revised April 19, 2018; accepted April 19, 2018
Abstract—The article discusses materials on the Archean (4.0–2.5 Ga) microfossils of the Earth (Greenland,
Australia, South Africa, and Fennoscandian Shield). The main emphasis is on the description of the finds of
possible members of eukaryotes. Analysis of the research by Russian paleontologists in this field has been car-
ried out.
Keywords: Archean, Precambrian, eukaryotes, acritarchs, bacteria, cyanobacteria, prokaryotes
DOI: 10.1134/S0031030119030043
INTRODUCTION
The Precambrian, or Cryptozoic, includes an
interval from the formation of the most ancient terres-
trial rocks known to date (approximately 4 Ga) to the
mass appearance of various skeletal organisms at the
Tommotian Stage base of the Cambrian. Although
the Precambrian (AR-PR) Period accounts for 85% of
the entire Earth’s history, and the Early Precambrian
(AR-PR1) Period exceeds 80% of the history of the
Earth, this period remained beyond the possibility of
studying by paleontologists for a long time.
This huge period of geologic time (almost 3.45 Ga)
is subdivided into two eons: Archean (2.5–4.0 Ga) and
Proterozoic (from 2.5 Ga to 530 Ma). At that time, the
biosphere was primarily microbial. Almost all Pre-
cambrian fossils may be divided into several catego-
ries: (1) microbial fossils, (2) stromatolites, (3) chem-
ical fossils, and (4) eukaryotes. Microbial fossils are
the remains of microorganisms enclosed in rock. Stro-
matolites are macroscopic biogenic-sedimentary for-
mations containing residues of fossilized microorgan-
isms. In a broad sense, chemical fossils include chem-
ical evidence of past life, which are biomarkers,
organic compounds, and biologically fractionated sta-
ble isotopes, e.g., carbon (Schidlowski, 1988, 2001,
2005; Schidlowski et al., 1979; Awramik, 1992).
The issue of the microbial taphonomy was first
mentioned by G.A. Zavarzin. Microbial communities
exist (and existed) under various conditions and,
depending on this, differ considerably. However, the
trophic relationships between the various groups of
microorganisms are similar in general terms. Organ-
isms develop individually or in small aggregates in
plankton communities. They transform into the fossil
state in the form of bottom sediments or coastal storm
release, where burial conditions are particularly favor-
able. Nevertheless, these taphocenoses do not reflect
the spatial structure of the natural community. The
probability of preservation of benthic communities is
the highest. In such burials (e.g., cyanobacterial
mats), their lifetime structure is often preserved
(Zavarzin, 1993).
Microorganisms, in general, and bacteria, in par-
ticular, are characterized by excellent preservation in
the fossil state, although, for a long time, microorgan-
isms were believed to be well preserved only in sili-
ceous rocks. It was first discovered by E. Barghoorn
and S. Tyler (Barghoorn and Tyler, 1965). Speaking
about the most ancient microorganisms, we always
mean fossilized, or fossil, microbes. Cell walls, cyto-
plasm, and glycocalyx (an extracellular polysaccharide
substance secreted by bacteria) are most susceptible to
mineralization. The material enriched with polysac-
charides easily chelates (binds) minerals. In this way
fossilization occurs, which often results in complete
replacement of organic matter by minerals, thereby
forming pseudomorphs.
Fossilization of microorganisms occurs incredibly
rapidly, often within a few hours (Westall et al., 1995;
Gerasimenko et al., 1996; Bakterial’naya…, 2002;
Rozanov, 2003, 2004; etc.). Rather abundant residues
of bacteria, and sometimes protists, are therefore rep-
resented exclusively by microfossils.
Involvement of bacteria in certain processes, such
as Fe and S accumulation (due to the activity of iron
and sulfur bacteria), was first discussed at the end of
the 19th century (1897) by N.I. Andrusov (Rozanov,
1999). After that, at the very beginning of the twentieth
century (in 1903), C. Leith suggested their biogenic ori-
gin while studying brown-red jaspilites (1.6–2.8 Ga)
(Antoshkina, 2011).
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ARCHEAN FOSSIL MICROORGANISMS 229
Comprehensive bacterial-paleontological studies
started in 1922, when V.I. Vernadsky came to the con-
clusion on the basis of the structure and geochemical
features of various sedimentary rocks. His conclusion
is the following: it is not possible to find any ancient
period in the geological history of the Earth, when the
formation of all sedimentary rocks known for that
perio d occur red in a delib erately abio genic way. More-
over, the Earth’s biosphere was formed as a complex
system from the very beginning, with a large number
of organism species, each of which fulfilled its role in
the common system. The biosphere could not exist at
all without this, i.e., the persistence of its existence
resulted from its complexity from the beginning (Ver-
nadsky, 1967).
A.G. Vologdin held the same views as Vernadsky.
Vologdin studied various rocks under a polarizing
microscope at high magnifications. These were rocks
of different ages (Proterozoic and Mesozoic): from
jaspilites to phosphorites and mineral formations of
the weathering zone. While Vologdin was studying
BIFs (jaspilites) of the Kursk Magnetic Anomaly, he
indicated the presence of iron bacteria in these rocks.
The author drew an unequivocal conclusion: the pres-
ence of massive bacterial or bacteria-like microbodies
in sedimentary rocks of any (including Early Protero-
zoic) age and in some secondary mineral formations is
unquestionable. There was no reason to consider them
as chemogenic formations; they had nothing in com-
mon with colloidal structures because of their rela-
tively large size (from 1 to 10 μm) (Volo gdin, 1947).
He named the field of his research geological micro-
biology.
Microbiologists were able to understand the ideas
of Vernadsky about the geological activity of microor-
ganisms only by the end of the 1950s. Thus, in 1959, an
article, the title of which completely repeated the title
of the Vologdin’s report at the meeting of the USSR
Academy of Sciences in 1947, was published
(Kuznetsov, 1959). Soon after that, a detailed mono-
graph of three authoritative microbiologists was pub-
lished (Kuznetsov et al., 1962). Vologdin wrote a
favorable review and summarized that the monograph
by S.I. Kuznetsov, M.V. Ivanov, and N.N. Lyalikova
had developed the groundwork for a new science, geo-
logical microbiology, which was at the edge of micro-
biology and geology (Vologdin, 1964). In turn, bacte-
rial paleontology (Rozanov and Zavarzin, 1997),
which was actually foreshadowed by Vologdin (Lapo,
2016), branched off geological microbiology in 1997.
The most ancient terrestrial rocks in which bio-
morphic microstructures are found are rocks of the
Archean greenstone belts of Western Greenland,
South Africa, and Australia (Knoll and Barghoorn,
1977; Schidlowski et al., 1979; Schopf, 1983, 1993;
Schidlowski, 1988, 2001, 2005; Knoll, 1994; and others).
The discovery of widespread fossilized microbial
residues in ancient sedimentary and volcanogenic sec-
tions suggests that their communities were the most
important factor in the evolution of the biosphere and,
above all, in sedimentation on the surface of the Earth,
starting from the Archean. Anaerobic bacteria began
functioning at least 3.5–3.8 Ga ago (Schidlowski,
198 8, 2001). Aerob ic bacter ia were al so regi stere d early
enough. Putative cyanobacteria are known from the
sediments aged approximately 3.5 Ga (Knoll and Bar-
ghoorn, 1977; Schopf, 1983, 1993; Knoll, 1994; Bak-
terial’naya…, 2002). The evidence for photosynthetic
life (both anoxygenic and oxygenic) dated earlier than
3.0 Ga ago, perhaps, 3.5–3.7 Ga (Rosing, 1999), was
also discussed.
At the end of the last century, the first works on the
most ancient sedimentary rocks of the Earth, the Isua
Greenstone Belt in Greenland, appeared as well. The
age of this belt is 3.8 Ga. The data on isotope analysis
of carbon in them suggested the existence of life
almost from the very beginning of the formation of
sedimentary rocks (3.8 Ga) (Schidlowski et al., 1979;
Schidlowski, 1988, 2001, 2005; Hayes, 1996; Mojzsis
et al., 1996; Rosing, 1999). These data have been crit-
icized many times, but have not been refuted. More-
over, they were confirmed by images of alleged bacte-
rial bodies from Isua, published by M. Schidlowski in
2005. Isotopic analysis performed by Schidlowski
indicated no fundamental difference between the res-
idues and microfossils from the Gunflint Formation
(2 Ga; Lake Superior, Canada) (Schidlowski, 2005);
and, most importantly, the presence of some residues
of eukaryotic algae in Isua (based on their isotopic
data) was assumed (Rozanov, 2017).
The models of the Late Archean Earth indicate a
variety of probable habitats for the most ancient
organisms (Nisbet, 2000). Under shallow coastal con-
ditions, communities of microbial mats can be
assumed, possibly with the participation of cyanobac-
teria, which carried out oxygenic photosynthesis. In
silts and bottom part of microbial mats, anoxygenic
photosynthetics and methanogens were probably
present. In the near-surface waters, photosynthetic
plankton probably flourished. Environment outside
the photic zone, inhabitants of which depended on the
geochemistry of sulfur, could also be common (Stet-
ter, 1996).
MICROBIAL FOSSILS
For a long time, the earliest life on the Earth was
considered to be in the form of the Early Archean fos-
sil bacteria found in sediments aged 3.3–3.5 Ga of the
Onverwacht Group of the Barberton Greenstone Belt
(South Africa) and the Warrawoona Group of the Pil-
bara Craton (Australia) (Lowe, 1980; Walter et al.,
1980; Schopf, 1983, 1993). Volcanogenic and volca-
nogenic-sedimentary rocks predominate in their sec-
tions. These Early Archean fossil bacteria are morpho-
logically indistinguishable from the modern bacteria.
From the evolutionary point of view, bacteria are
230
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ASTAFIEVA
organisms with rather complex organization and rep-
resent a high level of development (Bakterial’naya…,
2002). The earliest bacteria from the Barberton
Greenstone Belt of South Africa and Pilbara Green-
stone Belt of Australia probably developed microbial
mats on the surface of the sediment (Walsh, 1992).
Detailed sedimentological and micropaleontological
studies revealed a close relationship of microbial mats
with hydrothermal activity in shallow water (Bakte-
rial’naya…, 2002).
A. Knoll and E. Barghoorn (1977) discovered the
fossil community of organo-walled microstructures
while studying the Archean greenstone belt of Swazi-
land (~3.5 Ga, Mount Barberton, East Transvaal,
South Africa). Their dimension was within a rather
narrow range (1–4 μm, average diameter of 2.5 μm).
Their shape was not strictly spherical, but slightly flat-
tened and crumpled into folds. Moreover, various
stages of binary cell division were observed. The afore-
mentioned made it possible to suggest that the com-
plex of microfossils found had biogenic origin.
F. Westall discovered presumable bacterial (coc-
coid and rod-shaped) forms in the Barberton Green-
stone Belt (South Africa), which were completely
replaced by minerals (Westall et al., 2001).
Schidlowski (Schidlowski et al., 1979; Schidlowski,
2005) points at the duration of the biological process
of 3.8 Ga on the basis of analysis of the ratios of carbon
isotopes in the biogenic formations of Isua. Moreover,
this analysis suggests the presence of residues of highly
organized organisms for that time, such as eukaryotic
algae, in these sediments (Rozanov, 2009a, 2017).
Interesting molecular data indicating the existence
of cyanobacteria 2.7 billion years ago was obtained
(Brocks et al., 1999; Summons, 1999).
Similarly, the data on carbon and sulfur isotope
analysis support the conclusion that organic matter
was processed by bacteria in Archean sediments,
methanogens (microorganisms that produce meth-
ane) (Nisbet, 2000; Schidlowski, 2001), in particular,
and that the diverse chemotrophic community associ-
ated with hydrotherms existed in shallow (or medium
depth) basins. In 2000, B. Rasmussen published evi-
dence of the most ancient microbial life in volcanic
rocks aged 3.235 Ga. These were fossil filamentous
forms twisted in various directions, which were found
in massive sulfide sediments (Pilbara Craton, Austra-
lia). The author suggested that such type of sediments
was associated with the conditions characteristic of
black smokers. He suggested that these microorgan-
isms lived at the bottom of the Archean sea at high
temperatures below the photic zone (Rasmussen,
2000). This agrees with the optimal growth tempera-
tures of thermophilic bacteria (approximately 70°C).
High temperature is not a barrier for the development
of microbial life. Life can probably exist during under-
water eruptions, when the temperature of rocks
decreases below 113°C (Stetter et al., 1990; Stetter,
2006). In addition, cells of some methanogens are able
to reproduce under conditions of increased hydro-
static pressure at 122°C and a pressure of 20 MPa
(116°C require a pressure of 0.4 MPa) (Takai et al.,
2008). Moreover, the colonization of volcanic rocks
occurs wherever sea water can enter, which was shown
by the example of volcanic glass (Thorseth et al.,
2001). At the same time, microbial colonization of
both the surface of the substrate and the rock mass
occurs.
It should be noted that not all authors agreed on
the biological nature of the Archean remnants consid-
ered as fossil bacteria. Thus, M. Brasier et al. (2002,
2004) argued that the structures clearly resembling
well-preserved bacterial and cyanobacterial microfos-
sils from the Warrawoona Formation (~3.465 Ga) in
Western Australia (Schopf and Packer, 1987; Schopf
and Klein, 1992; Schopf, 1993, 1994), which were
considered one of the most ancient morphological
forms of life on Earth and which indicated the onset of
photosynthesis (Schopf, 1999), almost a billion year
older than putative cyanobacterial biomarkers (Sum-
mons et al., 1999), the appearance of oxygen atmo-
sphere (Catling et al., 2001), and any other relatively
diverse microbial communities (Schopf, 1999) are
actually contaminants, secondary artifacts formed
from amorphous graphite in multiple formations of
hydrothermal wedge and volcanic glass, or inorganic
carbon aggregates. They drew this conclusion after
repeated collection of material, mapping, optical and
electron-microscopic studies, digital image analysis,
Raman microspectroscopy, and the use of other geo-
chemical techniques. Subsequent work confirmed the
erroneous conclusions by Brasier and his co-authors,
and bacterial and paleontological studies of ancient
microorganisms continued fruitfully.
A.Yu. Rozanov (2003) suggested that fossils, the
biological nature of which Brasier doubted, could even
prove to be cyanobacteria forming cyanobacterial
mats. This conclusion by Rozanov agrees with his idea
of the early oxygenation of the atmosphere (~2.7 Ga).
V. Altermann and J. Kazmierczak (2003) after analyz-
ing the data by Brasier et al. and reassessing the prob-
ability of life on the early Earth, also concluded that
life in the Archean (2.5–3.5 Ga) was relatively wide-
spread and developed. This was done on the basis of
morphological, geochemical, and isotopic data. These
authors assumed that metabolic strategies were similar
to those in modern prokaryotic organisms, including
cyanobacteria. In their opinion, the oldest fossils of
the Earth are therefore microfossils aged 3.46–
3.49 billion years (Pilbara Craton, Western Australia)
and 3.4 billion years (Barberton region, South Africa).
The Archean microfossils of Western Australia and
South Africa can be considered as authentic ancient
fossils. It means that microbial life f lourished and was
widespread 3.5 billion years ago in the sediments stud-
ied by Schopf. The most ancient minerals in these
rocks are represented by spheroidal and filamentous
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ARCHEAN FOSSIL MICROORGANISMS 231
microfossils (Awramik et al., 1983; Walsh and Lowe,
1985; Schopf and Packer, 1987; Walsh, 1992; Schopf
and Klein, 1992; Schopf, 1993; Rasmussen, 2000;
Ueno et al., 2001). The debate of Schopf and Brasier
did not concern the findings in Isua, aged 3.8 billion
years (Schidlowski, 1988, 2001).
However, the paper by Brasier was a kind of a mile-
stone in the development of bacterial paleontology.
The turning point can be called the Schopf-Brasier
debate, which was followed by the beginning of a new
stage in the development of bacterial paleontology in
some countries.
At this stage of the development of bacterial pale-
ontology of the Archean, English-speaking research-
ers began to pay more attention to the chemical com-
ponent of the problem. Some authors, such as
F. Westall, almost entirely switched to astrobiology.
Nevertheless, many others remained true to the search
for traces of ancient life on the Earth. As a result, such
a change in the direction of work led to a diametrically
opposite result: the data on isotope analyzes of carbon,
sulfur, and oxygen, the distribution pattern of chemi-
cal elements, and petrographic analysis made it possi-
ble to postpone the first appearance of life on the
Earth to at least 3.8 Ga.
At the same time, along with isotopic and geo-
chemical studies, some researchers continued search-
ing for the most ancient microfossils as well.
STROMATOLITES
The interaction of microbial communities with the
environment, which occurs in the form of sedimenta-
tion and carbonate particle binding by microorgan-
isms with their subsequent lithification, results in the
development of stromatolites: layered organo-mineral
structures. Stromatolites are formed at the bottom of
warm shallow water reservoirs and in the tidal zone
(Maslov, 1960). The composition of microorganisms
determines the shape of their colonies, while the shape
of the colony is associated with the shape of stromato-
lite formations (Krylov, 1963). According to the shape
of the structure, stromatolites are subgrouped into
columnar, stratiform, and nodular stromatolites. Stro-
matolites were originally formed in the Early Archean
and were widespread in the Late Archean and Protero-
zoic. In the Late Archean, the areas occupied by stro-
matolites began to decrease, and there was their sharp
decrease in the middle of the Paleozoic (Komar, 1966;
Krylov, 1975; Walsh, 1992; Semikhatov and Raaben,
1994, 1996; Rozanov, 2009a; etc.). In the modern
world, microbial (chiefly cyanobacterial) structures,
which are formed under extreme conditions (e.g.,
Shark Bay in Australia and the Bahamas), are ana-
logues of the most ancient stromatolites (Iskopaemye…,
2011).
Stromatolites aged approximately 3.5 Ga were
found in Australia (Warrawoona group). A number of
works were devoted to interpretation of their origin.
D. Lowe (1980) suggested that Warrawoona stromato-
lites also owed their existence to cyanobacteria, since
the current stromatolites are predominantly composed
of cyanobacteria. However, some authors (Walter,
1972; Golubić, 1976; Walter et al., 1980) believed that
stromatolites probably arose due to the vital activity of
various microorganisms, since other types of prokary-
otes, as well as algae, are involved in the formation of
modern stromatolites. In particular, early Archean
stromatolites (e.g., Warrawoona Group; 3.5 Ga and
Onverwacht) are believed to be formed not by cyano-
bacteria, but by filamentous single-cell bacteria (pro-
karyotes) (Schopf, 1983). The Archean age of the stro-
matolites of Warrawoona indicates the existence of life
on the Earth at that time. The possible participation of
cyanobacteria in the development of stromatolites
(Lowe, 1980; Walter et al., 1980) suggests existence of
the photosynthetic process.
The collective monograph (Schopf, 1983), pub-
lished in 1983 and devoted to the early biosphere of the
Earth, attracted general attention and became one of
the most frequently cited papers. The main achieve-
ments of science were noted in this monograph:
(1) the possible origin of life was >3.8 Ga; (2) the
emergence of bacterial photosynthesis was >3.4 Ga
(bacterial photosynthesis) and the photosynthetic
release of O2 was possibly earlier than 3.8 Ga; and
(3) the appearance of eukaryotes was aged from 2.0 to
1.3 Ga. In the same monograph, all data on the most
ancient stromatolites (from the Early Archean)
obtained at that time were brought together. Accord-
ing to M. Walter, late Archean stromatolites were asso-
ciated with both brackish and marine conditions. In
the same monograph, J. Schopf and Walter tabulated
all the Archean microorganisms of stromatolites
known at that time with analysis of the reliability of
their in situ origin and the probability of biogenic ori-
gin. Early Proterozoic objects were analyzed by
H. Hofman and Schopf. An attempt to develop the
criteria for the in situ origin of discovered microfossils
and to provide images of microfossils from various
Archean and Proterozoic locations was made.
Over time, Schopf’s data were significantly cor-
rected by Rozanov (2004, Fig. 4; 2009b). Analysis of
various data showed that the first bacteria (s.l.)
appeared by the time of the termination of the meteor-
ite bombardment, i.e., approximately 4.0 Ga; the
presence of eukaryotes was shifted to 2.7–3.0 Ga. The
diversity and patterns of morphogenesis of Precam-
brian stromatolites and their comparison made it pos-
sible to consider that they owed their formation to cya-
nobacteria; and cyanobacteria, therefore, appeared
earlier than 3.5 Ga. Thus, paleontological and molec-
ular-biochemical data suggest that life on Earth
existed from the very beginning of sedimentation,
which raises the question of the origin of life with par-
ticular urgency.
232
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ASTAFIEVA
Relic microbial communities in extreme habitats
were comprehensively studied by L.M. Gerasimenko
et al. (1994). They pointed to the possibility of using
relict microbial communities in extreme habitats as a
model for their ancient ancestors. Among relict com-
munities of prokaryotes, cyanobacterial mats are of
the highest interest; they are usually compared with
flat stromatolites, which are believed to be unchanged
through the entire history of Earth, and their forma-
tion was caused by the microorganisms similar to the
modern ones (Krylov, 1975; Golubić, 1976; Schopf,
1983; Zavarzin, 1984). V.N. Sergeev (1993) believed
that cyanobacterial communities of the Early Protero-
zoic were almost similar to the modern ones. Appar-
ently, they successfully existed earlier, in the Archean.
Some filamentous forms of cyanobacteria transform
into the fossil state not as separate filaments, but as
scattered cells (Gerasimenko and Krylov, 1983).
According to Sergeev (1993), many forms of cyano-
bacteria have modern analogues at the genus or even
species levels.
Most of the known Early Archean bacteria may be
associated with flat microbial mats or biofilms (stro-
matolites of the stratiform type), and not with domical
or nodular stromatolites. The presence of such stro-
matolites in shallow water and tidal zone suggests that
microbial mats were formed by organisms for which
light was an important source of energy (e.g., photo-
synthesizing organisms). Coccoid, oval, and rod-
shaped bacteria, associated with the primary filamen-
tous mat builders, are heterotrophic or chemolytic
microorganisms (Bakterial’naya…, 2002).
While studying the most ancient stromatolites of
the Warrawoona Group (3.5 Ga), S. Awramic revealed
several morphotypes of filamentous fossil bacteria.
Based on the diversity of the ancient community and
the complexity of the individual components, he sug-
gested that the beginning of life on the Earth preceded
the beginning of the deposition of Warrawoona sedi-
ments (Awramic et al., 1983). The most ancient stro-
matolites of the Earth were also found in the Swazi-
land Supergroup in the Barberton Mountains (South
Africa), in the area with excellent outcrop of the most
ancient relatively weakly metamorphosed sedimentary
rocks. Spheroidal microfossils (several microns in
diameter) and double cells were found there, which
can be probable evidence of their reproduction by
binary division. The study of the Early Archean stro-
matolites indicated that the organisms that formed
them 3.5 Ga ago were benthic throughout their exis-
tence (or during most of their life). These bacteria
were probably photoautotrophic filamentous forms
with a cover around trichomes. The presence of stro-
matolites aged 3.5 billion years suggests that the
diverse microbial life existed on Earth even at that
time, grouping into microbial ecosystems. In the
absence of competition, cyanobacterial mats probably
occupied all ecological niches in the Precambrian
basins: from shallow water to the open sea (Awramic,
1971; Serebryakov, 1975). Based on the analysis of the
predominance of early Precambrian stromatolites, the
Earth, beginning with 3 Ga, was characterized by
widespread shallow-water marine conditions (Awra-
mik, 1992).
CHEMICAL FOSSILS
All deposits and forms that were considered bio-
genic on the basis of carbon and sulfur isotope analy-
ses can be assigned to fossils of this type (Schidlowski
et al., 1979; Schidlowski, 1988, 2001, 2005; Awramik,
1992).
In addition, N. Banerjee and his colleagues
(Banerjee et al., 2007) found interesting microfossils
in Archean pillow lavas (3.35 Ga, the Pilbara Craton,
Australia), which were micron-sized tubular struc-
tures mineralized with titanite (CaTiSiO4) with resid-
ual organic carbon preserved along their edges.
According to the data on U-Pb, the age of titanite in
tubular structures was Archean. These structures are
probably identical to the traces of the microbial activ-
ity in ophiolites and modern basalts. Moreover,
microbial activity facilitated biogenic leaching of
basalt glasses framing pillow lavas and hyaloclastites
(Furnes et al., 2004; Banerjee et al., 2006). Similar
microbial decomposition of basalt glasses was
recorded in well-preserved ophiolites and in the mod-
ern oceanic crust (Thorseth et al., 1992).
Biomarkers, or chemofossils, can also be assigned
to chemical fossils as well. The study of them is
extremely important. Thus, the data on the discovery
of sterols in the sediments aged 2.7 billion years
(Brooks et al., 1999) confirm the existence of eukary-
otes during that period. At the same time, the amount
of oxygen in the atmosphere should have been at least
1% of its present amount (the Pasteur point).
RECENT STUDIES
Perhaps, the most interesting discovery of recent
years is the location of metacarbonate rocks aged
3.7 billion years in the Isua Greenstone Belt. In these
sediments, the most ancient stromatolites (as high as
1–4 cm) were found. According to rare-earth element
analysis and yttrium traces, the Isua stromatolites were
formed in shallow water. Thus, fossil bacterial struc-
tures are found in greenstone belts from the very
beginning of the truly documented geological record
(Nutman et al., 2016).
Moreover, subsequent research confirmed the
existence of life on the Earth almost immediately after
the cessation of meteorite bombardment. There are
also some surprising and doubtful data that the first
traces of life were found in the sediments (the Nuv-
vuagittuq Greenstone Belt, Quebec, Canada), aged
over 3.77 billion years and can even approximate to
4.28 billion years (the precise age of the rocks was not
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ARCHEAN FOSSIL MICROORGANISMS 233
determined). These ferruginous sedimentary rocks are
interpreted as bottom sediments associated with
hydrothermal vents. Micron-sized hematite tubules,
morphologically similar to microbial filaments from
modern hydrotherms, were found in them. Graphite
granules, or carbon rings (carbonaceous material,
apatite, and carbonate rosettes) were found near the
tubules. Rosettes could be formed as a result of abio-
genic processes. However, apatite, which is an indirect
sign of the biological activity, was revealed along with
them. Carbon isotope analysis of graphite indicates
the presence of life. After all the data were analyzed
and merged, the existence of the microbial commu-
nity near hydrothermal vents in the Archean could be
discussed (Dodd et al., 2017).
M. Dodd and D. Papineau (2015) discovered ellip-
soidal formations of microcrystalline hematite in the
inclusions of ferruginous quartzites of the Nuvvuagit-
tuq Greenstone Belt (<3.8 Ga). Hematite roses were
preserved and almost not deformed, which indicates
that these structures were subjected to metamorphism
of low stages (not higher than greenschist). The excep-
tionally low degree of metamorphism of these Eoar-
chean rocks made it possible to preserve the randomly
located organic carbon with pyrite, apatite, carbonate,
and layered silicates. It also provided an opportunity to
search for possible traces of the most primitive life.
The use of Raman spectroscopy revealed the potential
biological nature of these formations.
On the basis of analysis of the ratio of carbon iso-
topes in graphites enclosed in the most ancient meta-
sedimentary rocks of Northern Labrador (Canada;
3.95 Ga), the following was established. Since graph-
ites have biogenic origin, living organisms existed
3.95 Ga ago (Tashiro et al., 2017). The data on traces
of the early life, which flourished in water basins at
least 3.7 Ga was confirmed by the morphology and
carbon isotope analysis in graphite grains of the Isua
schist (Schidlowski, 1988, 2001; Ohtomo et al., 2014).
Thus, the most ancient sedimentary rocks, the ori-
gin of which may be associated with the biological fac-
tor, were found in the Nuvvuagittuq Greenstone Belts
(Canada), Isua (Greenland), and the Akilia complex
(Greenland). All these rocks have lithological and
geochemical similarities (Mloszewska et al., 2013).
BIFs, which are associated with possible manifesta-
tions of life in all the most ancient sites, were suggested
to preserve both direct and indirect evidence of the
activity of the early microbial biosphere associated
with the intensive use of metals dissolved in seawater
(Mloszewska et al., 2013; Dodd and Papineau, 2015).
PROBABLE EUKARYOTES
D. Oehler and her colleagues have recently discov-
ered quite large (20–70 × 15–35 μm; measurements
by the authors) lentil-shaped forms with a rough
structure of the surface in the Archean Pilbara Craton
(Australia; aged 3.0–3.4 Ga). Carbon isotope analysis
of these forms was also carried out. The described
forms reminded the authors of the previously discov-
ered forms in the Archean of South Africa (the Barber-
ton Greenstone Belt; aged 3.4 Ga), which they inter-
preted as probable microorganisms. The comparison
of the morphology, spatial distribution, and facies of
the Australian and South African forms indicated that
these forms differed from other Early Archean micro-
fossils and that they could be related. These microor-
ganisms flourished in the early Archean seas; they
were abundant and widespread. They were probably
planktonic. It was suggested (based on the data of car-
bon isotope analysis) that lentil-shaped microorgan-
isms were probably autotrophs (Oehler et al., 2017).
The authors of the article did not go further than this
definition. The morphology of these forms and their
dimensions suggest that they could be the earliest
eukaryotes.
Organ-walled microfossils aged 3.2 billion years
were found in shallow-water sediments, and more spe-
cifically, in Early Archean schists and siltstones of the
Moodies Group of the Barberton Greenstone Belt
(South Africa). This is a fossilized population of large
(up to 300 μm in diameter) carboniferous spheroidal
microstructures. Isotope and chemical (Raman
microspectroscopy) analyses were performed. Based
on these analyses and careful morphological analysis,
as well as analysis of probable conditions of sedimen-
tation, the authors suggested that these microfossils
were associated with cyanobacteria, although they
were much larger than all the known cyanobacteria
(Javaux et al., 2010). However, R. Buik (2010)
assigned these large spheroidal forms to acritarchs,
i.e., to eukaryotes, while exploring the same mate-
rial. We share his opinion.
RUSSIAN RESEARCH
Among the most ancient rocks in the territory of
Russia are Middle Archean (2.9–3.0 Ga) siliceous
sedimentary rocks: silicites of the Hautovaara and Koy-
kara structures of the Vedlozero-Segozersky Green-
stone Belt (Central Karelia, Fennoscandian Shield).
Conducted bacterial-paleontological studies (Svetov
and Medvedev, 2012; Medvedev et al., 2014) revealed
traces of biofilms and microstructures, considered fos-
silized, chiefly filamentous, microorganisms.
However, the first reliable findings of fossilized res-
idues of the members of eukaryotes in the Archean
were described by B.V. Timofeev in 1982. He
described the acritarchs and large trichomes from the
Upper Archean deposits of Central Karelia and the
Middle Dnieper (Timofeev, 1982). For a long time,
this work remained the only one in which the Archean
findings of fossilized remains of the members of
eukaryotes, including acritarchs, were recorded.
However, this work was almost unnoticed and, more-
234
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ASTAFIEVA
Plate 1
12
34
5
78
6
10 µm
30 µm10 µm
3 µm
3 µm
10 µm3 µm
10 µm
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ARCHEAN FOSSIL MICROORGANISMS 235
over, the possibility of finding eukaryotic forms in
Archean sediments is still doubtful.
In order to confirm or confute Timofeev’s conclu-
sions, we reexamined his collection, which is stored in
the Institute of Geology and Geochronology of the
Precambrian (Russian Academy of Sciences), and
collected and studied additional material from the
Archean of North Karelia (Khizovaar Greenstone
Structure; 2.8 Ga), which is part of Parandovsko-Tik-
shozerskiy Greenstone Belt. Samples from the volca-
nogenic-sedimentary association of the middle and
acid composition of the bottom part of the section
were studied. As a result of the research, prokaryotic
forms were primarily found; presumable eukaryotic
fossil microorganisms were also revealed (Astafieva
et al., 2005, 2006; Astafieva, 2006; Rozanov et al.,
2008; Rozanov and Astafieva, 2013, etc.)
In the section (in carbonaceous schists and tuff-
sedimentary rocks), filamentous and rod-shaped
forms prevailed. Most of these structures were repre-
sented by filaments with a diameter of the order of 3–
5 μm (as a rule), the length of which reached (or even
exceeded) 100 μm (Pl. 1, figs. 1–4). According to the
morphology and size, Archean filamentous structures
can also be referred to cyanobacteria. It should be
noted that a structure resembling a cyanobacterial mat
was found in one sample (Pl. 1, fig. 4).
The coccoid forms in the Lopian rocks of
Khizovaar were also found in both carbonaceous
schists and tuff-sedimentary rocks. These forms were
represented by several modifications. First, rather
peculiar coccoid forms were revealed in carbonaceous
schists, tuff sandstones (sandstones with admixture of
volcanic material of acidic composition), as well as tuff-
sedimentary and sedimentary rocks. These cocci were
round forms (a diameter of approximately 2–5 μm)
that almost always formed clusters (Pl. 1, fig. 5). The
surface of these spheres was covered with a kind of
rather dense and thick fluffy sheath enclosing each
coccus separately. Some samples had cracks in this
cover. The presence of such an ornamented sheath is
characteristic of both prokaryotes and eukaryotes.
However, it should be noted that there is a possibility
that accumulations of these forms may be a later con-
tamination.
Second, single cocci, which had uneven tuberous
surface (3–4 μm in diameter) and were interspersed
into the rock, were revealed (Pl. 1, fig. 6).
Third, these are larger spherical forms with a diam-
eter of approximately 10 μm (Pl. 1, figs. 7, 8). They are
particularly interesting that they are represented by
cocci (consisting mainly of silicon and iron) with a
very rough (bumpy) surface. In some cases, these coc-
coid forms are covered with a rather thick uneven
bumpy bubble shell (sheath or cover), in the chemical
composition of which iron abruptly prevails.
This sheath is presumably nothing more than iron-
rich glycocalyx, which covered these forms when they
were alive. There is another, somewhat less probable,
assumption that iron-rich cover was a secondary for-
mation that could be associated with the activity of
endoliths. The probable internal structure of these
coccoid formations is shown in Pl. 1, fig. 8 and indi-
cates a rather complex organization of these forms.
Forms with complex organization, covered with
lamellar plates, were also found in tuff-sedimentary
rocks. These microorganisms probably belonged to
eukaryotes. However, judging by the interrelation with
host rocks, the probability of the later contamination
is very high.
In the weathering crusts of granites and plagiog-
ranites of North Karelia, another supposedly eukary-
otic form of an uncertain systematic position was
found (Astafieva and Rozanov, 2010), the interpreta-
tion of which was difficult. Later, some similarity of
the described form with the testate amoebas was noted
(Rozanov and Astafieva, in press). It is a half-
destroyed elongated oval microfossil. Nevertheless,
taking into account its Archean age, it can be consid-
ered as quite well preserved. Its dimensions were as
follows: length ~57 μm and width ~17 μm. This form
had a rather complex organization; it was probably
covered with a sheath as thick as 2–3 μm (Pl. 2, fig. 1).
It was found in the pre-Upper Lopian weathering
crust (AR, the basis of the Okhta Group, ~2.8 Ga;
Voronye Lake, the Lekhta Structure of Karelia).
Explanation of Plate 1
All the depicted specimens originated from the Archean (2.8 Ga) Khizovaar Greenstone Structure (North Karelia).
Figs. 1–4. Filamentous forms of Archean carbon-containing schists: (1, 2) filamentous forms; images under a CamScan-4 elec-
tron microscope nos. 1020 and 1027 dated February 22, 2005; (3) filamentous intertwining forms disrupted in the central part of
the image; such a gap suggests that a crack in the rock was formed after fossilization of the filaments; image under a CamScan-4
electron microscope no. 1023 dated February 22, 2005; (4) structure resembling a layer of cyanobacterial mat of tuff-sedimentary
rocks; image under a CamScan-4 electron microscope no. 00030 dated November 30, 2004.
Figs. 5 and 6. Coccoid forms from tuff-sedimentary rocks: (5) agglomeration of coccoids; an image under a CamScan-4 electron
microscope no. 10007 dated January 26, 2005; (6) single forms; image under a CamScan-4 electron microscope no. 00020 dated
October 25, 2005.
Figs. 7 and 8. Coccoid forms with a rough surface from tuff-sedimentary rocks: (7) coccoid forms covered with a rough sheath;
image under a CamScan-4 electron microscope no. 0021 dated October 25, 2005; (8) an enlarged fragment showing the complex
internal structure of the coccoid form in Fig. 7.
236
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ASTAFIEVA
1
3 4
5
7 8
6
2
10 µm
3 µm
10 µm
10 µm
20 µm2 µm
3 µm
Plate 2
10 µm
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ARCHEAN FOSSIL MICROORGANISMS 237
Weathering crust of Voronye Lake also contains
prokaryotic fossil microorganisms. Among them, fila-
mentous, rod-shaped, dumbbell-shaped, and coccoid
forms are present (Iskopaemye…, 2011) (Pl. 2, f igs. 2, 3).
The discovery of microfossils with complex organi-
zation from the core of the well drilled on the western
flank of the Imandra-Varzuga rift belt (the Kola Pen-
insula) should also be noted. The well opened the
weathering crust with an age of >2.448 Ga, i.e., almost
on the boundary of Archean and Proterozoic. Accord-
ing to the morphology, the fossils discovered belonged
to multicellular eukaryotes, probably red or green
algae. The characteristics of the described fossil forms
closely resembled those of some modern representa-
tives of the genera Draparnaldia and Draparnaldiella
(green algae) (Kursanov, 1953; Moshkova, 1986;
Vodorosli…, 1989). These are branched shrub-shaped
forms with pronounced differences between the main
threads and the lateral branches, although sometimes
vertical threads prove to be intensively developed.
They are attached to the substrate by rounded-oval
flattened bases, which look like bottle-shaped forms
or rounded-flattened patches in electron images
(Pl. 2, figs. 4, 5). It should, however, be noted that the
possibility of the fungal nature of the fossils found
cannot be completely excluded. These forms were
named Gazavarzinia (Rozanov and Astafieva, 2013).
The results of the study of fossil microbes show that
mineral formation under their effect or with their par-
ticipation is a process, which took place on the Earth
at all times and everywhere (Rozanov and Astafieva,
2009). As already mentioned, fossil bacteria were
found in most ancient meta-sedimentary rocks. But
the role of bacteria in ancient sedimentation and min-
eral formation has not been studied enough. Thus, an
attempted study of the Archean BIFs of North Kare-
lia, the Kola Peninsula, and India showed that the bio-
logical factor played a certain role in the formation of
these mineral resources. In all studied samples of the
Early Archean BIFs, microfossils were found both in
the ferruginous and siliceous interlayers. The most
abundant and diverse forms, which are close to coc-
coids, are cocci and oval, dumbbell-shaped, rod-
shaped and other forms; biofilms are abundant (Pl. 2,
figs. 5–8). The microbial forms of Archean BIFs are
quite diverse. Part of the detected microfossils may be
remnants of magnetotactic and iron-reducing bacte-
ria. Thus, the bacterial component probably partici-
pated in the formation of the Archean ferruginous
quartzites. Most likely, the Archean seas were warm-
water pools not rich in oxygen. In other words, the
Archean ferruginous quartzites seem to be among the
most ancient biogenic rocks (Astafieva et al., 2017).
CONCLUSIONS
Thus, we can say that life on our planet appeared
almost at the beginning of the geological record. This
ancient life was represented by bacteria and probably
by archaea (it is impossible to morphologically distin-
guish these groups in the fossil state). The presence of
cyanobacteria, and therefore the process of photosyn-
thesis, is not excluded. The presence of eukaryotes
already in the Archean (even in the Eoarchean), much
earlier than the traditional period of their appearance,
is also noted. Modern bacterial-paleontological stud-
ies have changed our understanding of the most
ancient stages of the evolution of life on the Earth.
Microbial communities in ancient sedimentary and
volcanogenic sections were proved to be the most
important factor in the evolution of the biosphere and,
Explanation of Plate 2
Figs. 1–3 originate from the Archean (Lopian, 2.8 Ga) weathering crusts (Voronye Lake, the Lekhta Structure, Karelia).
Fig. 1. Elongated oval shape, the length and width of which exceed 50 and 15 μm, respectively. This form has a rather complex
structure, probably covered with a sheath with a thickness of 2–3 μm; this form can be assigned to eukaryotes (the data are not
enough for a more accurate conclusion). The image under a CAMSCAN-4 electron microscope no. 1433 dated March 25, 2008.
Fig. 2. A fragment of rock consisting of fossilized biofilm with filamentous, rod-shaped and coccoid forms; image under a
CAMSCAN-4 electron microscope no. 0030 dated March 17, 2008.
Fig. 3. A fragment of rock consisting of destroyed cocci, dumbbell-shaped forms, and fragments of threads, coated with biof ilm;
an image under a CAMSCAN-4 electron microscope no. 0029 dated March 17, 2008.
Figs. 4 and 5. Fossilized algal-shaped forms of Gazavarzinia kolae Rozanov et Astafieva, 2013 from Lower Proterozoic (2.45 Ga)
weathering crusts of Imandra-Varzuga rift belt (Kola Peninsula): (4) general view, image under a Zeiss electronic microscope
no. 1236 dated November 24, 2009; (5) round-oval flattened base, by means of which forms are attached to the substrate; a Zeiss
electron microscope image no. 1237 dated November 24, 2009.
Figs. 6–8. Archean microfossils (>2.7 Ga) of the Olenegorsk Structure of the Murmansk oblast of Kola Peninsula: (6) numerous
small (D ≤ 0.5 μm) round-oval shapes, probably immersed in fossilized glycocalyx; image under a Zeiss electron microscope
no. 3200 dated November 19, 2012. The chemical composition of these forms is dominated by iron, so there could be doubts
about the biogenicity of their origin. However, many microorganisms (prokaryotes and even eukaryotes) accumulate various met-
als (e.g., the Witwatersrand gold ore deposit, which is the largest in the world (2.35–2.4 Ga) and in which the formation was
according to bacterial mats) (Shkol’nik et al., 2005; Iskopaemye…, 2011); (7) small cocci are numerous, randomly scattered in the
rock, sometimes form small clusters or chains; fragments of the rock, which are almost entirely composed of small cocci (round-oval
formations), are also found. In the left part, small cocci are immersed in the rock; in the right part, they are under the cover of bio-
film; interlacing of filamentary and rod-shaped forms is traced, which confirms the lifetime burial of the remains. Image under a
Zeiss electron microscope no. 3100 dated November 9, 2012; (8) elongated oval or rod-shaped forms; their length is 2–3 μm, their
width is 1.0–1.5 μm. They are often grouped together, forming threadlike structures, the question of their origin is debatable.
Image under a CamScan-4 electron microscope no. 2207 dated September 05, 2012.
238
PALEONTOLOGICAL JOURNAL Vol. 53 No. 3 2019
ASTAFIEVA
above all, sedimentation on the surface of the Earth,
starting with the Archean.
Moreover, the presence of fossil bacteria and,
probably, even eukaryotes in the Archean weathering
crust suggests that terrestrial life existed in such
remote times. Therefore, it does not seem entirely cor-
rect to assert that life appeared in the ocean.
ACKNOWLEDGMENTS
The author thanks everyone who helped to carry
out this work, for discussing the results and valuable
advice, especially A.Yu. Rozanov and G.T. Usha-
tinskaya, as well as L.V. Zaitseva, R.A. Rakitov, and
A.V. Kravtsev for their assistance in the studies with
electron scanning microscopes.
FUNDING
This work was supported by the Program no. 17 of
the Presidium of the Russian Academy of Sciences
(“The Evolution of the Organic World. The Role and
Influence of Planetary Processes”; Subprogram I
“Development of Life and Biospheric Processes”)
and by the Russian Foundation for Basic Research
(project no. 17-04-00324).
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Translated by A. Panyushkina
