Morphological record of oxygenic photosynthesis in
conical stromatolites
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Bosak, Tanja et al. “Morphological record of oxygenic
photosynthesis in conical stromatolites.” Proceedings of the
National Academy of Sciences 106.27 (2009): 10939-10943. ©
2009 National Academy of Sciences
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http://dx.doi.org/10.1073/pnas.0900885106
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United States National Academy of Sciences
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Morphological record of oxygenic photosynthesis
in conical stromatolites
Tanja Bosak1,2, Biqing Liang1, Min Sub Sim, and Alexander P. Petroff
Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139
Edited by Paul F. Hoffman, Harvard University, Cambridge, MA, and approved May 15, 2009 (received for review January 27, 2009)
O
xygenic photosynthesis irreversibly changed the Earth’s
surface environment by using light energy to split water and
evolve molecular oxygen (Eq. 1)
CO2 ⫹ H2O 3 O2共g兲 ⫹ CH2O.
The timing of the evolution of this metabolism is controversial
(1–7), but it must have predated the geochemical record of initial
oxygenation of the atmosphere at 2.4 billion years ago (Ga) (8).
The sedimentary record of photosynthetic microbial communities is at least 1 billion years older (9) and commonly written in
the laminated and lithified sedimentary structures called stromatolites. Conical stromatolites are a distinct morphological
group that, to date, lacks plausible abiotic analogs, but the
metabolic provenance of their microbial builders remains difficult to establish even in structures much younger than 2.4 Ga.
Modern conical stromatolites are thought to owe their distinct
shape to biological processes because thin filamentous cyanobacteria are known to form small cones (10) even in the complete
absence of lithification. Light is essential for the growth of
cyanobacterial biomass in modern cone-building biofilms (10).
The upward migration of phototactic filaments is thought to be
another mechanism contributing to the vertical growth of modern cones (10), although it remains unclear whether this vertical
growth is due to phototaxis or simply to the enhanced growth at
the tips of cones. Once a conical structure forms, models
suggests that the fast vertically accreting mat may propagate the
shape through successive laminae in the presence of fast lithification (11).
Models assuming an enhanced accumulation of biomass at
topographic highs (11) or the vertical orientation of long filaments at the tips of stromatolites (10) can account for the
thickening of the laminae in the centers of conical stromatolites
(12). Yet, these models cannot account for other common
characteristics of the crestal zone, a prominent but poorly
understood internal feature defining an entire class of Paleo- and
Mesoproterozoic conical stromatolites that formed in quiet
zones outside the influence of waves and storms (12) (Fig. 1A).
The crestal zone often has contorted or discontinuous laminae,
some of which appear to have enclosed submillimeter- to milliwww.pnas.org兾cgi兾doi兾10.1073兾pnas.0900885106
Bubble Formation at the Tips of Modern Conical Structures
Light is critical both for the growth of photosynthetic coneforming cyanobacteria (10) and as a determinant of the resulting
morphology of biofilms (Fig. S2). Although ridged or flatter
structures grow at higher light intensities, low-light conditions
enhance the growth of prominent cones with axes inclined in the
direction of light (Fig. S2). Higher photosynthetic activity in the
tips of these cones (Fig. 2B), in turn, often leads to the formation
of oxygen-rich bubbles in our enrichment cultures but not on the
sides of cones (i.e., in the zones of highest photosynthetic activity
under light-limiting conditions). These bubbles, colonized by a
mesh of filamentous cyanobacteria, are generally much smaller
than cones and do not confer a conical shape onto the mat.
Bubbles are either clearly visible (Fig. 2 A) or can be detected in
cross-sections of modern lithifying cones as submillimeter- and
millimeter-diameter features with nearly-circular cross-sections
(i.e., completely enclosed by laminae) (Fig. 2C and Figs. S3 and
S4). Bubbles surrounded by a thick, actively photosynthesizing
mesh can grow into irregularly shaped blisters, disrupt the
laminae (Fig. 2C and Fig. S5) or initiate the growth of millimeter- to centimeter-diameter tubes.
If mechanically and gravitationally stable bubbles are to form,
to persist, and to become preserved by fast lithification, they
should be smaller than ⬇5 mm in diameter and heavily enmeshed. The recognition of fossil bubbles as features with
nearly-spherical cross-section will then be possible if the surrounding microbial mesh is preserved by sufficiently small
crystals (i.e., smaller than the average lamina thickness), and if
significant recrystallization does not occur. In modern hot
springs (14) and in our cultures that contain less than ⬇2 mM
inorganic carbon, only bubbles smaller than ⬇0.2 mm are
enclosed by a thick mesh (Fig. S3). Larger nearly-spherical
bubbles in these environments will be enclosed by a much more
porous or discontinuous mesh of filaments and not necessarily
preserved or identifiable. Bubbles that form in the centers of
very narrow central zones (⬍200 ␮m) would be similarly difficult
to preserve and recognize. In deeper waters, at lower photosynAuthor contributions: T.B., B.L., and M.S.S. designed research; T.B., B.L., M.S.S., and A.P.P.
performed research; T.B., B.L., M.S.S., and A.P.P. analyzed data; and T.B. and B.L. wrote the
paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1T.B.
2To
and B. L. contributed equally to this work.
whom correspondence should be addressed. E-mail: tbosak@mit.edu.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0900885106/DCSupplemental.
PNAS 兩 July 7, 2009 兩 vol. 106 兩 no. 27 兩 10939 –10943
MICROBIOLOGY
cyanobacteria 兩 microbialite
meter-sized bubbles (13) [Fig. 1 and supporting information (SI)
Fig. S1]. Using enrichment cultures of modern cone-forming
cyanobacteria from Yellowstone National Park, here, we test the
influence of light on the centimeter- to submillimeter-scale
external and internal morphology of cyanobacterial cones and
link the formation of oxygen-rich bubbles in the tips of modern
cyanobacterial cones to the fossil gas bubbles present in the
central zone of modern, Proterozoic, and even some Archean
conical stromatolites.
GEOLOGY
Conical stromatolites are thought to be robust indicators of the
presence of photosynthetic and phototactic microbes in aquatic
environments as early as 3.5 billion years ago. However, phototaxis alone cannot explain the ubiquity of disrupted, curled, and
contorted laminae in the crests of many Mesoproterozoic, Paleoproterozoic, and some Archean conical stromatolites. Here, we
demonstrate that cyanobacterial production of oxygen in the tips
of modern conical aggregates creates contorted laminae and submillimeter-to-millimeter-scale enmeshed bubbles. Similarly sized
fossil bubbles and contorted laminae may be present only in the
crestal zones of some conical stromatolites 2.7 billion years old or
younger. This implies not only that cyanobacteria built Proterozoic
conical stromatolites but also that fossil bubbles may constrain the
timing of the evolution of oxygenic photosynthesis.
Fig. 1. Center of a conical stromatolite [Atar Formation, Atar Group, Mauritania, Late Mesoproterozoic (53, 54), sample provided by A. Maloof]. (A) Mosaic
photomicrograph of the central zone (thin section). The white rectangle surrounds the area shown in B, and the arrows point to fossil bubbles. (Scale bar, 1 cm.)
(B) A typical nearly-circular submillimeter feature surrounded by dark laminae in the middle of the stromatolite (white arrow). This fossil bubble is found on top
of a larger, irregularly shaped feature surrounded by contorted laminae (outlined by a dashed line) that may be a former mat-trapped bubble. (Scale bar, 1 mm.)
(C) Fossil bubbles are absent from laminae on the sides of the same conical stromatolite. (Scale bar, 1 mm.) (D) Histogram showing the diameters (in millimeters)
of fossil bubbles in 18 well-preserved Proterozoic conical stromatolites. Bubbles were identified as submillimeter- and millimeter-diameter features with
nearly-circular cross-sections enclosed by laminae.
thetic rates, or in solutions rich in dissolved inorganic carbon,
however, even millimeter-scale photosynthetic bubbles will be
extensively covered by a microbial mesh and more likely to be
preserved by syngenetic mineralization (Figs. S4, S5, and S6).
Bubbles in Proterozoic Conical Stromatolites
Nearly-circular features enclosed by contorted laminae are
primarily observed at the tips of some well-preserved Proterozoic conical stromatolites but not on the sides (Fig. 1 and Fig.
S1). The analogy with modern laminated cones suggests that
these circular features originated as submillimeter- to millimeter-sized gas bubbles. The localization of millimeter-scale contorted laminae in conical stromatolites to the topographic highs
implies that those were the spots of active in situ production of
gas, whereas the absence of fossil bubbles on the sides of conical
stromatolites suggests that the local gas concentration was not
sufficient to create bubbles. Areas enclosed by contorted and
sometimes disrupted laminae (12) in the crests of conical
stromatolites are thus a likely consequence of gas release
resulting from higher microbial metabolic activity on the topographic highs (Fig. 1 and Fig. S1). These inferred gas bubbles in
coniform stromatolites can occupy anywhere from 0% to ⬇20%
of the central zone (13).
Discussion
The presence of cone-forming cyanobacteria can easily explain
the growth of bubbles enclosed by primary laminae in the crests
of conical stromatolites and the accumulation of sufficient gas to
overcome considerable hydrostatic pressure at depth (more than
twice the atmospheric pressure at 10 m). On the other hand,
light-independent microbial production of gases such as H2,
CH4, CO2, CO, and H2S, N2O, and N2 require abundant organic
matter or high concentrations of nitrate in the solution, the latter
requiring the presence of atmospheric oxygen. Unlike oxygen
bubbles that give a circular shape to the laminae formed by
primary producers at the top of the structure (Fig. 2 and Fig. S4),
fenestrae originating from the decay of unmineralized organic
matter in rapidly accreting tips tend to destroy the primary
lamination and tend to have irregular shape distributions (e.g.,
ref. 15). In contrast, the inferred bubbles in conical stromatolites
are restricted only to the crests even in the very narrow (millimeter-wide) central zones (Fig. S1), where they do not disrupt
the surrounding laminae. The degradation of organic matter by
methanogenic microbes can produce bubbles at large depths (16)
that, coupled with methanotrophy, can lead to the precipitation
of large-scale carbonate structures with central vents. These
carbonate structures differ from conical stromatolites because
Fig. 2. Oxygen and bubble production in modern conical aggregates dominated by cyanobacteria. (A) Bubbles often form at the tips of cones and are partly
or completely covered by biofilm. Note that these bubbles did not lift the mat up into a conical structure. (Scale bar, 5 mm.) (B) Profiles of oxygen (filled circles)
and gross photosynthetic rate (white bars) and oxygen uptake rate (gray bars) within a cone. Depth 0 mm denotes the tip of the cone and ⫺6 mm is the bottom
of the cone. (C) Transmitted-light micrograph of a 30-␮m-thick thin section of a cone showing disrupted fabrics, large voids (former blisters), and bubbles in the
center. Multiple pores surrounded by cyanobacterial filaments were present in the series of successive thick sections, confirming that the porosity was not an
artifact. The sample had an elliptical cross-section, and it was sectioned along the minor axis. (Scale bar, 1 mm.)
10940 兩 www.pnas.org兾cgi兾doi兾10.1073兾pnas.0900885106
Bosak et al.
Table 1. Presence of contorted laminae, a distinct axial zone, and bubble-like structures in Archean conical stromatolites
Age, Ga*
Contorted laminae and/or
distinct axial zone
Cement-filled contorted laminae
(possible fossil bubbles)
3.4
Absent
Absent
3.1–2.9
3.0–2.8
2.9–2.7
2.8 ⫾?
2.7
2.7
Absent
Unclear‡
Unclear§¶
Probably absent储
Present
Present
Absent
Unclear‡
Unclear§¶
Probably absent储
Present
Present**
2.7–2.6
Unclear¶
2.7
2.6–2.9
2.7–2.6
Poorly defined and
narrow
Present
Present
Present
2.7–2.6
⬍2.63
2.63–2.52
Unclear¶
Unclear¶
Present
Unclear¶
Unclear¶
Present
Present
Unclear¶
Present
Reference†
Allwood et al., 2007 (37); Hofmann
et al., 1999 (38); Lowe, 1980 (39)
Beukes and Lowe, 1989 (40)
Hofmann et al., 1985 (41)
Wilks and Nisbet, 1985 (42)
Donaldson and deKemp, 1998 (43)
Hofmann and Masson, 1994 (23)
Sakurai et al., 2005 (44); Van
Kranendonk et al., 2006 (25)
Grey, 1981 (45)
Hofmann et al., 1991 (24)
Srinivasan et al., 1990 (46)
Walter, 1983 (47); Abell et al., 1985
(48)
Lambert, 1998 (49)
Murphy and Sumner, 2008 (50)
Beukes, 1987 (26); Buck, 1980 (51);
Altermann, 2008 (27)
Continent
Australia
Africa
North America
North America
North America
North America
Australia
Australia
North America
Asia
Africa
North America
Australia
Africa
*Ages based on the references listed in table 1 in Schopf (52) and Hofmann (28).
†References only given for the sources that contain detailed descriptions and/or images of conical stromatolites.
‡Biogenicity and stromatolitic nature questionable (41).
¶Insufficient detail given in the published pictures or preserved.
§Stromatolites are poorly preserved.
储Insufficient detail given in the published picture.
**Contorted laminae consistent with the former presence of a bubble can be seen in the middle of a well-developed central zone can be seen in Van Kranendonk
et al. (25), although we are not aware of any published photographs showing a thin section.
Bosak et al.
MICROBIOLOGY
conical stromatolites as early as 2.7 Ga (23–25) and in more
widespread cones on Late Archean carbonate platforms (26, 27)
(Table 1 and Fig. 3). The apparent absence of fossil bubbles in
the few Archean cones older than 2.7 Ga (Table 1 and Fig. S7)
may be attributed both to poor preservation and to a very small
number of described conical stromatolites (28), but further
experiments are needed to determine whether these cones could
have grown in the presence of anoxygenic photosynthetic microbes. The origin of gas-related features in Archean conical
stromatolites thus deserves focused investigation because these
features may be the first detectable traces of oxygen exhaled
under an anoxic atmosphere that forever changed the surface
environment on our planet.
GEOLOGY
the former lack continuous laminae, their porosity is not spatially
restricted to topographic highs, and they contain carbonate
minerals exhibiting characteristically depleted carbon isotopes
(17) that are not observed in well-preserved stromatolites (18).
The presence of methanogens in communities with anoxygenic
photosynthetic microbes could potentially account for the largescale conical shape of stromatolites, and, possibly, the localization of bubbles at the tips. This model is unlikely because
anoxygenic phototrophs and methanogens actually compete for
substrates in some modern environments (19), suggesting that
intense production of methane should not be expected in the
zones of highest photosynthetic activity. Moreover, processes
such as microbial iron and sulfate reduction and fermentation
would be energetically better poised to degrade of organic
matter close to the photosynthetic layer in the thin bubbleenclosing laminae, diminishing the likelihood of abundant methane production. Although further search for cone-building and
gas-producing anaerobic photosynthetic communities is warranted, such communities are not known currently. We also note
that hydrogen-based anoxygenic photosynthesis would take up
H2 and CO2, thereby reducing the local concentration of gases
needed to form bubbles. Overall, stromatolite growth in the
presence of strongly phototactic cyanobacteria best accounts for
the presence of inferred fossil bubbles at the tips of nondivergent
conical stromatolites.
Gas-bubble entrapment has been suggested as the origin of
axial porosity in the central zone of some Proterozoic stromatolites (13). Here, we explicitly link the photosynthetic production of oxygen to the deformed laminae commonly observed in
the central zones of Proterozoic conical stromatolites (12, 13, 20,
21). Cyanobacteria were thus involved in the formation of some
well-preserved Paleoproterozoic and Mesoproterozoic cones as
well as some much younger Neoproterozoic conical stromatolites (22). Intriguingly, features consistent with fossil bubbles and
contorted laminae in the crestal zone may be present in rare
Fig. 3. Some of the oldest conical stromatolites with possible bubble-like
features in the central zone. (A) Central zone of a conical stromatolite from
Lime Acres Formation at Lime Acres, Griqualand, South Africa (2.52–2.55 Ga)
(21) (Scale bar, 2 mm.) (B) Small diapirs surrounded by contorted laminae at
the crests of a conical stromatolite from the Meentheena Member of the
Tumbiana Formation, Australia (⬇2.7 Ga) (25).
PNAS 兩 July 7, 2009 兩 vol. 106 兩 no. 27 兩 10941
Materials and Methods
Culturing Media and Growth Conditions. Cone-forming cyanobacteria from
Yellowstone National Park were obtained under the permit number YELL2008-SCI-5758 from National Park Services. Two cyanobacterial clones dominate the 16s rDNA clone libraries from our enrichment cultures. One of these
sequences (GenBank accession no. FJ933259) is 99% similar to a sequence
found in cone-forming mats in Yellowstone National Park (29), whereas the
other one is 97% similar to a sequence reported from mats growing at
50 –55 °C in Yellowstone (30). The cultures were grown on solid substrate
(agar, silica sand, or aragonite sand) at 45 °C in modified Castenholz D medium
(31) containing lower concentration of nitrate and phosphate (2.3 mM NO3⫺
and 0.8 mM PO43⫺, respectively) at pH 8. The medium was initially in equilibrium with an atmosphere of 5% CO2, 5% H2, and 90% N2, although coneforming cultures grow well even in the medium equilibrated with air. The
cultures were grown at various distances from a fluorescent cold light source
with a 12-h day–12-h night cycle, and the medium was exchanged periodically
(every week). Lithification in the medium was promoted by lowering phosphate concentration to 80 ␮M and 0.23 mM NO3⫺ and increasing calcium and
magnesium concentration to 3.5 mM and 4 mM, respectively, by the addition
of CaCl2 and MgCl2. The initial pH of the lithifying medium was 7.6, and sterile
medium prepared in this manner did not contain visible precipitates.
Microscopy. Samples were removed from actively growing cultures by a sterile
surgical blade, fixed with 2.5% glutaraldehyde dissolved in 0.1 M sodium
cacodylate (pH 7.4) for 2 h. After the fixative was washed away, the samples
were embedded in Sakura TissueTek O.C.T. compound (VWR), frozen for at
least 2 h, and sectioned to a thickness of 30 –50 ␮m at ⫺20 °C by using a
cryostat (Leica). O.C.T. was washed away by 0.1 M sodium cacodylate buffer
and imaged by using epifluorescence, differential interference contrast and
phase contrast modules on an Axio Imager M1 epifluorescence microscopy
(Zeiss).
diameter tip with a guard cathode (32) at an irradiance of 180 ␮E/m2/s. The
microsensors were calibrated at the experimental temperature (45 °C) and
salinity. Diffusive flux of oxygen was calculated by using Fick’s first law of
1-dimensional diffusion and steady-state profile of oxygen (33).
Jz ⫽ DedC z/dz
where De is an effective diffusion coefficient and dCz/dz is the slope of the
microprofile at depth z. De in the bacterial colony was assumed to be 1.6 ⫻
10⫺5 cm2/s (34). Therefore, the net photosynthetic rate in a specific layer can
be determined from the balance between oxygen fluxes through the overlying and underlying areas.
Gross photosynthetic rate was measured by using the same sensor and the
light– dark shift method (35). In the steady state, the photosynthetic oxygen
production is equal to the loss of oxygen due to respiration and to diffusion.
After the termination of illumination, the photosynthesis stops instantaneously, whereas diffusion and respiration are initially unchanged. This assumption should be valid as long as the decrease in oxygen concentration is
linear with time (36). We measured the decrease in oxygen concentration
within 5 s after the darkening and calculated the oxygen uptake (respiration)
rates from the difference between the net and gross photosynthetic rates.
Supporting Information. For more information, see SI Text.
Measurement of Oxygen Profiles and Photosynthetic Rate. Oxygen concentration was determined by using a Clark-type oxygen microsensor with a 25-␮m-
ACKNOWLEDGMENTS. A. Maloof (Princeton University) and S. Ono (Massachusetts Institute of Technology) provided the samples of Proterozoic and
Archean conical stromatolites; A. Theriault and J. Dougherty enabled the
analysis of the Geological Survey of Canada samples; G. Geesey and S. Gunther
assisted with field work in Yellowstone National Park; S.-H.D. Shim and G.
Brent helped with Raman spectroscopy; D. Rothman, H. Hofmann, S. Golubic,
B. Weiss, J. Kirschvink, V. Sergeev, 3 anonymous reviewers, and members of
the Massachusetts Institute of Technology Laboratory for Geomicrobiology
and Microbial Sedimentology provided useful comments; T. Grove (Massachusetts Institue of Technology) and S. Bowring (Massachusetts Institute of
Technology) provided the rock saw and the petrographic microscopes; and J.
Barr generously assisted with the cutting.
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