LETTERS
PUBLISHED ONLINE: 17 NOVEMBER 2013 | DOI: 10.1038/NGEO2005
Potential influence of sulphur bacteria on
Palaeoproterozoic phosphogenesis
Aivo Lepland1,2,3 *, Lauri Joosu4 , Kalle Kirsimäe4 , Anthony R. Prave5 , Alexander E. Romashkin6 ,
Alenka E. Črne1,7 , Adam P. Martin8† , Anthony E. Fallick9 , Peeter Somelar4 , Kärt Üpraus4 ,
Kaarel Mänd4 , Nick M. W. Roberts8 , Mark A. van Zuilen10 , Richard Wirth11 and Anja Schreiber11
Corg (wt%)
P2O5 (wt%)
0
5
10
15
0
δ13Corg (%% VPDB)
20 40 60 ¬38
¬36
¬34
6.5
6.0
Height above outcrop base (m)
All known forms of life require phosphorus, and biological
processes strongly influence the global phosphorus cycle1 .
Although the record of life on Earth extends back to 3.8 billion
years ago2 and the advent of biological phosphate processing
can be tracked to at least 3.5 billion years ago3 , the earliest
known P-rich deposits appeared only 2 billion years ago4,5 .
The onset of P deposition has been attributed to the rise
of atmospheric oxygen 2.4–2.3 billion years ago and the
related profound biogeochemical shifts6–9 , which increased
the riverine input of phosphate to the ocean and boosted
biological productivity and phosphogenesis5,10 . However, the
P-rich deposits post-date the rise of oxygen by abour
300 million years. Here we use microfabric, trace element
and carbon isotope analyses to assess the environmental
setting and redox conditions of the 2-billion-year-old P-rich
deposits of the vent- or seep-influenced Zaonega Formation,
northwest Russia. We identify phosphatized microorganism
fossils that resemble modern methanotrophic archaea and
sulphur-oxidizing bacteria, analogous to organisms found in
modern seep settings and upwelling zones with a sharp
redoxcline11,12 . We therefore propose that the P-rich deposits
in the Zaonega Formation were formed by phosphogenesis
mediated by sulphur bacteria, similar to modern sites13 , and by
the precipitation of calcium phosphate minerals on microbial
templates during early diagenesis.
Precipitation of phosphate phases in sedimentary rocks is
typically achieved in the diagenetic environment close to the
sediment–water interface. Microbial degradation of organic matter
and reductive dissolution of Mn- and Fe-oxyhydroxides resulting
in release of scavenged phosphate are often considered as the main
processes generating the interstitial concentrations needed for the
formation of calcium phosphate mineral apatite1 . Involvement of
sulphur-metabolizing microbial communities mediating calcium
phosphate precipitation was suggested for the Miocene Monterey
Formation in California14 , and this was confirmed by studies
of organic-rich sediments on continental margins11,13 as well as
laboratory experiments13,15 that, combined, showed that bacterially
mediated, redox-dependent P-cycling provides an important sink
for marine P and phosphorite formation in general.
5.5
5.0
4.5
4.0
Organic-rich mudstone
Dolostone
Figure 1 | Geochemical profiles through the phosphate-rich interval of the
Zaonega Formation exposed in a ∼10-m-thick outcrop at Shunga village.
Abundances of P2 O5 and Corg and isotopic composition of Corg were
determined on bulk samples.
Several species of sulphur-oxidizing bacteria, (for example
Beggiatoa, Thiomargarita, the latter being the largest known
bacterium with reported size up to 750 µm) have a high
1 Geological
Survey of Norway, 7491 Trondheim, Norway, 2 Tallinn University of Technology, Institute of Geology, 19086 Tallinn, Estonia, 3 Centre for Arctic
Gas Hydrate, Environment and Climate, University of Tromsø, 9037 Tromsø, Norway, 4 University of Tartu, Department of Geology, 50411 Tartu, Estonia,
5 Department of Earth and Environmental Sciences, University of St Andrews, St Andrews, KY16 9AL Scotland, UK, 6 Institute of Geology, Karelian Science
Centre, Pushkinskaya 11, 185610 Petrozavodsk, Russia, 7 Ivan Rakovec Institute of Paleontology, ZRC SAZU, SI-1000 Ljubljana, Slovenia, 8 NERC Isotope
Geosciences Laboratory, British Geological Survey, Keyworth, Nottingham NG12 5GG, UK, 9 Scottish Universities Environmental Research Centre, Rankine
Avenue, Scottish Enterprise Technology Park, East Kilbride, G75 0QF Scotland, UK, 10 Géobiosphère Actuelle et Primitive, Institut de Physique du Globe de
Paris – Sorbonne-Paris Cité, Université Paris Diderot, UMR 7154, CNRS, 1 rue Jussieu, 75238 Paris cedex 5, France, 11 GeoForschungsZentrum Potsdam,
Telegrafenberg, Chemistry and Physics of Earth Materials, D-14473 Potsdam, Germany. † Present address: GNS Science, Private Bag 1930, 9054 Dunedin,
New Zealand. *e-mail: [email protected]
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NATURE GEOSCIENCE DOI: 10.1038/NGEO2005
LETTERS
a
b
c
d
e
f
Figure 2 | SEM images and element maps of phosphate nodules, layers
and lenses. a–f, SEM–backscattered electron (BSE) image (a) and
SEM–energy-dispersive spectrometry (EDS) element maps of P (b), C (c),
Ca (d), Si (e) and Mg (f). Phosphate nodules, layers and lenses (high P and
Ca) occur in carbonaceous mudstone containing phlogopite (high Si and
Mg) and carbonaceous matter (high C). Scale bars, 800 µm.
capacity for storing polyphosphate13 . These bacteria operate
at the (sub)oxic–sulphidic interface where they thrive in close
association with a consortium of anaerobic methane-oxidizing
archaea and synthropic sulphate-reducing bacteria and gain energy
from the oxidation of H2 S and other reduced-sulphur species
using O2 or NO−
3 . When conditions become sulphidic, the stored
polyphosphate is hydrolysed and phosphate can be released into
sediment pore water triggering Ca-phosphate precipitation on
nucleation templates that may include cell membranes16 .
Deeper in time, during the Palaeoproterozoic era (2.5–1.6 billion
years ago; Ga), seawater sulphate concentrations increased in
response to oxygenation of Earth7 , and we propose that it was
then that the environmental conditions were established that
favoured the activity of both sulphur-reducing and -oxidizing
microorganisms to generate the 2.0 Ga phosphogenic episode. An
exemplar of that episode is the Zaonega Formation in the Onega
Basin, Karelia, Russia, a ∼1,500-m-thick succession of organic-rich
sedimentary rocks interlayered with mafic tuffs and lavas and
containing several P-rich layers in its upper part (Supplementary
Information). The Zaonega Formation’s age is constrained to
∼2.06–1.98 Ga based on whole-rock and mineral Sm–Nd and
Pb–Pb isochrons on a gabbro body in the overlying Suisari
Formation17 , and by the underlying Tulomozero Formation, which
records the Lomagundi–Jatuli carbonate carbon isotope excursion
that terminated in Fennoscandia 2.06 Ga (ref. 18). The Zaonega
Formation contains numerous thick, syn-depositional lavas, sills
and peperites (brecciated rock formed by the emplacement of
sills into wet, unconsolidated sediment). These are evidence for
a magmatically active setting and their emplacement would have
generated temperatures sufficiently high in proximity to the igneous
2
bodies for sediments to pass through the oil window (60–120 ◦ C).
They also triggered the generation and migration of hydrocarbons,
petroleum seepage, asphalt spilling19 and fluid circulation, and
the inferred expulsion of both high- and low-temperature vents
and seeps. Subsequent greenschist facies (∼400 ◦ C) overprinting
occurred during the 1.89–1.79 Ga Svecofennian orogeny.
We sampled the P-rich rocks of the Zaonega Formation from
outcrop and in cores obtained by the Fennoscandian Arctic
Russia—Drilling Early Earth Project (FAR-DEEP; Fig. 1 and
Supplementary Fig. 2). A particularly P-rich, 2-m-thick mudstone–
dolostone interval was targeted for detailed study and was sampled
in outcrop at Shunga village (Fig. 1), about 300 m northwest of
FAR-DEEP drillhole 13A (Supplementary Fig. 1). Phosphates occur
in both dolostones and organic-rich (30–70 wt% of total organic
carbon) mudstones, typically forming impure layers, lenses and
nodules consisting mainly of carbonaceous matter, fluorapatite
(hereafter apatite) and phlogopite (Fig. 2 and Supplementary
Fig. 3). Phlogopite is interpreted to represent an alteration product
of original sedimentary Mg(Fe)-rich clay derived from either
weathered mafic–ultramafic rocks or hydrothermal fluids and was
later transformed by diagenesis/metamorphism.
Carbonaceous matter associated with layers having increased
P2 O5 concentrations (>1 wt%) in the upper-middle part of the
Zaonega Formation has relatively light C-isotopic composition,
with δ13 C Vienna Pee Dee Belemnite (VPDB) values ranging
from −38 to −30h (Supplementary Fig. 2)9,19 . In contrast, the
δ13 C values from the P-poor lower part of the formation span
from −30 to −20h. The samples obtained from outcrop have
δ13 C values from −37 to −34h (Fig. 1). The occurrence of
strongly 13 C-depleted carbonaceous matter in the middle-upper
part of the Zaonega Formation has been attributed to the presence
of methanotrophic biomass and the influence of CH4 -carrying
vents and seeps19 . Many of the mudstones are characterized
by sub-millimetre-scale lamination that commonly displays a
wrinkly crinkly fabric, including features such as roll-ups and
microscale folding indicating cohesiveness and pliability, and in rare
instances convex-up laminae defining millimetre-amplitude domal
structures. We interpret this fabric as preserved microbial mats,
many of which are marked by high carbonaceous matter content
(Figs 2 and 3c), again consistent with a vent/seep-influenced setting
in which abundant productivity of chemosynthetic biomass is commonplace. Furthermore, Zaonega sediments underlying the P-rich
interval have been interpreted as accumulating in predominantly
euxinic (anoxic and sulphidic) conditions experiencing redox
fluctuations20 . Distinctly increased, but highly variable abundances
of redox-sensitive Mo and U in the P-rich upper part of the Zaonega
Formation recorded in the FAR-DEEP cores (Supplementary Fig. 2)
are consistent with fluctuating redox states and episodes of oxic
conditions to allow Mo and U mobility21 .
Petrography and scanning electron microscopy (SEM) reveals
that the phosphates commonly appear as clustered or individual
round–oval nodules that are, in places, agglomerated into layers
(Fig. 3 and Supplementary Fig. 4). Nodule sizes mostly range from
200 to 1,000 µm (mean 336 µm), but can be as large as 3,000 µm
(Supplementary Figs 5 and 6). Many are flattened and deformed
(Fig. 3b), indicating that they were soft during early burial. Some
nodules are associated with organic-rich mudstone laminae that
deflect around their margins (Fig. 3c), which further demonstrates
their early diagenetic formation, pre-dating lithification.
In the phosphate nodules and P-rich layers, apatite occurs
as cylindrical particles with consistent diameters of ∼0.5–4 µm
and lengths of ∼1–8 µm (Fig. 4a–d and Supplementary Figs 4
and 7), and rarely as spherical aggregates as big as 5 µm in
diameter (Fig. 4e–f). These particles and aggregates are dispersed
in a carbonaceous matrix, and neighbouring layers and nodules
can have highly variable apatite-to-matrix proportions. SEM
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NATURE GEOSCIENCE DOI: 10.1038/NGEO2005
a
1 mm
b
1 mm
c
1 mm
Figure 3 | SEM–BSE images of phosphate nodules and layers from
polished rock slabs. a–c, Nodules occur as clustered (a,b) and isolated (c)
in laminated mudstones and are commonly deformed and flattened (b).
Fine lamination deflects around nodules as shown in c, indicating early
diagenetic formation. Variable backscatter intensity of individual nodules
and lenses is owing to different proportions of impurities, mainly
carbonaceous matter, but also phlogopite. Light phases on images are
owing to relatively strong backscatter response of apatite compared with
the matrix sediment that is rich in carbonaceous matter.
and transmission electron microscopy (TEM) of best-preserved,
least-recrystallized apatite cylinders reveal that the internal parts
consist of anhedral apatitic aggregates and carbonaceous matter
(Figs 4b and 5a–e) whereas the outer perimeter is rimmed by apatite
crystallites 100–300 nm in size and showing ordered alignment
(Fig. 5c). The apatitic aggregates in the interior of cylinders contain
nanometre-scale inclusions (Fig. 5b), the composition of which is
unknown at present.
Such high-quality preservation is rare though, and most cylinders are partly to entirely recrystallized, displaying preferential
crystallite alignment along the longer axis of cylinders. In these
instances, the recrystallized apatite cylinders have a radial inner structure (Fig. 4c) and/or hexagonal appearing crystal habit
(Fig. 4d). It is noteworthy that neither the initial shape nor size
LETTERS
of the apatite cylinders was significantly affected by recrystallization. The carbonaceous matter surrounding apatite cylinders is
structurally better ordered at the contacts forming ∼30-nm-thick
graphitic films (Fig. 5c). Such graphitic films result from preferential graphitization of carbonaceous matter on mineral surfaces
(mineral-templated graphitization) during metamorphism22 .
Preservation of the microbial fabric in ancient phosphogenic
settings including those from the Palaeoproterozoic has been
documented previously23 . Formation of cylindrical apatite particles
has been interpreted as resulting from biologically mediated
nucleation in pore water, though the mechanisms have been poorly
understood24 . Apatite coatings are recognized as moulds formed
from precipitation around coccoidal and rod-shaped microbes24 .
Oval to ellipsoidal phosphatic particles rimmed with clay-rich
cortices (authigenic smectites and Fe–Si–Al amorphous phases)
have been observed in stromatolite-building bacterial communities
and are interpreted as moulds of apatite crystallized from an amorphous Ca-phosphate precursor precipitating on bacterial walls25 .
Interpretation of mineralized bacterial cells25 is consistent with
experimental results that demonstrate massive mineralization of
microbial colonies by Ca-phosphate precipitation and no precipitation outside the colonies16 . Furthermore, cell membranes have been
experimentally shown to serve as initial templates for Ca-phosphate
nucleation with the mineralization continuing towards the cell
interiors16 . Similarly, we propose that the formation of the outer rim
of the aligned apatite crystallites seen in the best-preserved cylinders
documented herein, was initiated by nucleation on cell membranes
that acted as highly reactive surfaces and nucleation templates,
probably occurring when the cells were metabolically active. Apatite
nucleation seems to have continued during the post-mortem stage
resulting in the interior of cells also becoming mineralized.
The apatite cylinders and spherical aggregates in the Zaonega
Formation have shapes and sizes similar to the methanotrophic
archaea ANME-1 and ANME-2 (ref. 26), which inhabit microbial
mats in modern venting and seepage areas where they operate in
close associations with sulphate-reducing and sulphur-oxidizing
microbial communities26 . Thus, based on form and inferred
palaeoenvironmental setting, we interpret the apatite cylinders
and spherical aggregates in the Zaonega Formation as fossilized
phosphatized methanotrophic archaea. The uniform size of the
apatite cylinders is likewise consistent with a biogenic precursor
rather than a purely inorganic precipitation of apatite crystallites,
which would have resulted in variable shapes and sizes.
Typical sizes and form of the phosphatic nodules are similar to those of giant sulphur-oxidizing bacteria (for example,
Thiomargarita), known from modern13 and controversially also
from ancient27,28 phosphogenic settings, although some of the
Zaonega nodules are larger. Given that these bacteria are known
to mediate phosphogenesis, we conclude that the nodules are
fossilized sulphur-oxidizing bacteria. Thiomargarita cells are prone
to collapse easily29 , hindering their preservation in the rock record,
unless stabilized by coeval mineral precipitations around the cells;
we infer this was the case in the Zaonega Formation, resulting in the
fossilization of the sulphur-oxidizing bacteria nodules.
The presence of inferred phosphatized methanotrophs in the interior of nodules implies that a consortium of microorganisms was
functioning within the Zaonega environments. Our interpretation
is that, on death of the sulphur-oxidizing bacteria, methanotrophs
colonized the interior of the cell and were themselves subsequently
phosphatized in the early diagenetic environment, thereby further
preventing the collapse of original nodular cell walls. Such a
scenario (that is, activity of methanotrophs post-dating the sulphur
oxidizers) is expected from the diagenetic sequence of thermodynamically determined oxidant depletion, in which oxygen and
nitrate used by sulphur oxidizers are depleted at shallower depths
relative to sulphate, which is used by anaerobic methanotrophs.
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NATURE GEOSCIENCE DOI: 10.1038/NGEO2005
LETTERS
c
b
a
2 µm
1 µm
1 µm
d
e
f
2 µm
2 µm
2 µm
Figure 4 | SEM–BSE images of cracked rock surfaces illustrating apatite particles (BSE light) and the massive carbonaceous matrix (BSE dark) in
phosphate nodules and layers. a–f, Apatite occurs as variably recrystallized cylindrical particles with consistent diameters and lengths (a–d) and spherical
aggregates (e, f), similar to the methanotrophic archaea ANME-1 and ANME-2 (ref. 26).
b
a
500 nm
b
1 µm
c
Film of graphitic carbonaceous matter
Poorly ordered
carbonaceous matter
Ordered alignment of
apatite crystallites
d
500 nm
e
500 nm
500 nm
Figure 5 | TEM images of a 100-nm-thick foil generated by focused ion beam milling. a, HAADF detector image of apatite (bright) cylinders in the matrix
of carbonaceous matter (dark). Note the heterogeneous composition of the internal parts of cylinders and more homogeneous apatite rims at perimeters.
b, HAADF close-up image of apatite cylinder illustrating the co-occurrence of apatite (light) and carbonaceous matter (dark) in the internal parts and
presence of ∼5–20 nm inclusions in apatite (ubiquitous grey dots). The composition of these inclusions is unknown at present. c, Bright field image of an
apatite cylinder showing the occurrence of apatite crystallites with ordered alignment at the perimeter and the presence of a film of graphitic carbonaceous
matter22 surrounding the cylinder. d,e, Electron energy loss spectroscopy jump ratio images of calcium (d) and carbon (e) from the area shown in c. Bright
contrast represents the higher abundance of the analyte. Calcium and carbon are both present in the internal part of the cylinder tracking the
co-occurrence of apatite and carbonaceous matter respectively, whereas carbon is largely absent from the rim where aligned apatite crystallites occur.
Geochemical characteristics and morphological features of
P-rich intervals in the Zaonega Formation are consistent with
sulphur-bacteria-mediated phosphogenesis and Ca-phosphate
4
precipitation on microbial templates during early diagenesis.
This can be linked to microbial communities cohabited by a
consortium of sulphur metabolizers and methanotrophs inhabiting
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NATURE GEOSCIENCE DOI: 10.1038/NGEO2005
seep/vent-influenced environments. The increase in seawater
sulphate concentration during the Palaeoproterozoic oxygenation
of Earth probably enhanced the activity of sulphur metabolizers and
allowed, for the first time, significant sulphate reduction in sediments, build-up of pore-water H2 S and establishment of (sub)oxic–
sulphidic redoxclines at shallow sediment depth, consistent with
the appearance of carbonate concretions at the time30 . Even though
the phosphogenesis in the Zaonega Formation occurred in isolated
seep/vent-influenced sedimentary environments, it is possible
that other Palaeoproterozoic sedimentary environments may have
hosted phosphogenesis5 where sharp redoxclines developed in
response to changes in the sulphur cycle triggered by oxygenation
of the Earth. However, it was not until the increase in oxygen levels
during the Neoproterozoic that the environmental conditions were
established to enable widespread phosphogenesis.
Methods
SEM imaging and elemental mapping of samples was carried out at Tartu
University on a variable pressure Zeiss EVO MA15 SEM equipped with
Oxford X-MAX energy dispersive detector system and AZTEC software
for element analysis. Samples were studied both in freshly broken surfaces
perpendicular to bedding and in polished slabs embedded in epoxy resin.
Focused ion beam sample preparation using the FEI FIB 200-TEM and TEM
using FEI TecnaiG2 F20 X-TWIN were carried out at GeoForschungsZentrum
Potsdam. The TEM was equipped with a Gatan imaging filter (Tridiem),
EDAX X-ray analyser and a Fishione high-angle annular dark-field detector
(HAADF). Abundances of reported major elements were determined at ACME
Analytical Laboratories using inductively coupled plasma atomic emission
spectrometry (for P2 O5 ) and Leco elemental analyser (for Corg ). Carbon
isotope analysis of decarbonated powdered samples was carried out at the
Scottish Universities Environmental Research Centre using an elemental
analyser continuous flow isotope ratio mass spectrometry (ThermoScientific
Delta V Plus with Costech TC/EA). The 13 C/12 C ratios are reported as
δ13 C values in per mil relative to the 13 C/12 C ratio of the VPDB standard
(δ13 Csample = [(13 C/12 C)sample /(13 C/12 C)standard − 1] × 1,000). A more detailed
description of methods is given in the Supplementary Information.
Received 31 May 2013; accepted 14 October 2013; published online
17 November 2013
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Acknowledgements
This study was undertaken in the frame of the FAR-DEEP and was supported by the
International Continental Drilling Program, Geological Survey of Norway, Centre for
Geobiology of Bergen University, Norwegian Research Council grant 191530/V30,
Estonian Science Foundation grants ESF8774 and SF0180069S08 and Natural
Environment Research Council grant NE/G00398X/1. We thank V. A. Melezhik for
coordinating the FAR-DEEP, M. Mesli for managing the FAR-DEEP sample archive and
L. Kump for providing unpublished carbon isotope data on FAR-DEEP core 13A.
Author contributions
A.L. and K.K. conceived the study; A.E.R., A.L., L.J., A.R.P., A.E.Č. and A.P.M. carried
out field work and sample collection; L.J., K.K., P.S., K.Ü., K.M., N.M.W.R., A.P.M. and
A.L. carried out mineralogic, petrographic geochemical analyses; A.E.F. and L.J. carried
out carbon isotope analyses, R.W., M.A.v.Z., A.S., L.J., K.M. and A.L. carried out TEM
analyses. All authors contributed to the interpretation of results and the writing and
editing of the manuscript.
Additional information
Supplementary information is available in the online version of the paper. Reprints and
permissions information is available online at www.nature.com/reprints. Correspondence
and requests for materials should be addressed to A.L.
Competing financial interests
The authors declare no competing financial interests.
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