Download Formation and diagenesis of modern marine calcified cyanobacteria

Geobiology (2009), 7, 566–576
DOI: 10.1111/j.1472-4669.2009.00216.x
Formation and diagenesis of modern marine calcified
cyanobacteria
N. PLANAVSKY,1,2 R. P. REID,1 T. W. LYONS,2 K. L. MYSHRALL3 AND P. T. VISSCHER3
1
Rosenstiel School of Marine and Atmospheric Sciences, Miami, FL, USA
Department of Earth Sciences, University of California, Riverside, Riverside, CA, USA
3
Department of Marine Sciences, University of Connecticut, Groton, CT, USA
2
ABSTRACT
Calcified cyanobacterial microfossils are common in carbonate environments through most of the Phanerozoic,
but are absent from the marine rock record over the past 65 Myr. There has been long-standing debate on the
factors controlling the formation and temporal distribution of these fossils, fostered by the lack of a suitable
modern analog. We describe calcified cyanobacteria filaments in a modern marine reef setting at Highborne
Cay, Bahamas. Our observations and stable isotope data suggest that initial calcification occurs in living cyanobacteria and is photosynthetically induced. A single variety of cyanobacteria, Dichothrix sp., produces calcified
filaments. Adjacent cyanobacterial mats form well-laminated stromatolites, rather than calcified filaments, indicating there can be a strong taxonomic control over the mechanism of microbial calcification. Petrographic analyses indicate that the calcified filaments are degraded during early diagenesis and are not present in well-lithified
microbialites. The early diagenetic destruction of calcified filaments at Highborne Cay indicates that the absence
of calcified cyanobacteria from periods of the Phanerozoic is likely to be caused by low preservation potential as
well as inhibited formation.
Received 30 January 2009; accepted 11 April 2009
Corresponding author: N. Planavsky. Tel.: (951) 827-3127; fax: (951) 827-4324; e-mail: [email protected]
INTRODUCTION
Calcified cyanobacteria microfossils are a common component of marine carbonate reefs and sediments deposited from
550 to 100 Ma (Riding, 2000; Arp et al., 2001). Calcifiedmicrofossils morphologies are diverse, and many have been
assigned formal taxonomic names (Riding, 2000). Filamentous taxa, such Girvanella are likely the most common calcified cyanobacteria, and have a morphology that can be directly
related to modern cyanobacteria. These once common fossils
are absent from the marine rock record since the Late Cretaceous (Sumner & Grotzinger, 1996; Arp et al., 2001; Riding
& Liang, 2005).
Modern calcified cyanobacteria that are morphologically
comparable to ancient marine counterparts are commonly
found in freshwater settings and have been extensively studied
(e.g. Merz, 1992). However, since freshwater systems have
carbonate and other major ion compositions that are dramatically different from those of marine settings, these modern
calcified cyanobacteria are not direct analogs for ancient
566
marine cyanobacterial microfossils (Knoll et al., 1993; Dupraz
et al., in press). Calcified cyanobacteria are found in several
marine environments (Winland & Matthews, 1974; Hardie,
1977; Riding, 1977; MacIntyre et al., 1996), but there has
not been an extensive study of the calcification mechanisms in
any of these occurrences. The lack of a suitable, well-studied
modern analog for ancient marine calcified cyanobacteria has
fostered long-standing debate on the factors controlling the
formation, temporal distribution, and abundance of these
microfossils (Knoll et al., 1993).
The formation of calcified cyanobacterial microfossils is ultimately caused by a local increase in calcium carbonate saturation state driven by microbial metabolic activity. It has been
heavily debated if this shift in carbonate saturation state is
induced by cyanobacterial photosynthesis or heterotrophic
microbial metabolisms (Visscher et al., 1998; Riding, 2000;
Arp et al., 2001; Dupraz & Visscher, 2005; Dupraz et al., in
press). Uptake of carbon dioxide during cyanobacterial
photosynthesis increases the pH surrounding the cyanobacterial cell, which favors carbonate precipitation. Bicarbonate is
2009 Blackwell Publishing Ltd
Modern marine calcified cyanobacteria
the product of microbial sulfate and nitrate reduction, and its
production also promotes calcium carbonate precipitation
(see Morse & MacKenzie, 1990; Dupraz & Visscher, 2005;
Visscher & Stolz, 2005; Dupraz et al., in press for extensive
reviews of the effects of different microbial metabolisms on
calcium carbonate saturation state). These modes of calcified
cyanobacteria formation – photosynthetic and organic matter
remineralization induced carbonate precipitation – have typically been viewed as part of a binary system (Turner et al.,
2000; Arp et al., 2001; Kah & Riding, 2007). It has become
increasingly clear that extrapolymeric substances (EPS) produced by cyanobacteria and heterotrophic bacteria also play a
key role in calcification (e.g. Decho, 2000; Braissant et al.,
2007, 2009). Freshly produced EPS can have an inhibitory
effect on calcification through binding of cations (e.g., Ca2+,
Mg2+; Dupraz & Visscher, 2005). When the cation-binding
capacity is saturated (Arp et al., 2003), or when EPS is
degraded through microbial and ⁄ or physicochemical processes, large amounts of Ca2+ ions are released, promoting calcification (Dupraz & Visscher, 2005).
The factors controlling the temporal distribution of calcified cyanobacteria are also debated. Calcified cyanobacteria
first appear in rock record in the middle Precambrian (Kah
& Riding, 2007), but show a major increase in abundance
in the early Cambrian (Arp et al., 2001). This Cambrian
event may have been caused by cyanobacterial evolution or
major changes in the marine carbonic acid system (Walter &
Heys, 1985; Knoll et al., 1993; Turner et al., 2000; Arp
et al., 2001; Riding & Liang, 2005). Calcified cyanobacteria
are abundant through the most of the Paleozoic, but are
rare or absent for periods in the Mesozoic. Notably, calcified
cyanobacteria are rare in the Permian and Early Jurassic,
despite the presence of microbial carbonates during this
time period. Arp et al. (2001) proposed that the rarity of
mid-Mesozoic calcified cyanobacteria is linked with low
marine calcium concentrations. Calcified cyanobacteria are
rare in the Cretaceous and disappear from the marine rock
record in the Late Cretaceous. Their absence over the past
65 Ma is thought to be due to low marine calcium or
carbonate ion concentrations, which would have lowered
the calcium carbonate saturation state and inhibited microfossil formation (Sumner & Grotzinger, 1996; Riding,
2000; Arp et al., 2001).
Here we describe calcified cyanobacterial filaments from a
modern marine setting at Highborne Cay in the Bahamas. We
document the growth and early diagenetic history of the
calcified cyanobacteria at Highborne – presenting information
from field observations, petrographic examinations, and stable
isotope work. Our documentation of a modern marine calcifying cyanobacterium allows us to test models that explain the
formation, temporal distribution, and abundance of ancient
calcified cyanobacteria. Our study strengthens the view that
understanding the geochemical dynamics of modern
microbial ecosystems is essential to link microbial processes
2009 Blackwell Publishing Ltd
567
with sediments in the geological record and to understand the
evolution of microbial carbonate production.
STUDY AND LOCATION AND ENVIRONMENT
The calcified-cyanobacteria filaments are located in an open
marine environment at Highborne Cay (7649¢W, 2443¢N)
Exuma, Bahamas. Tufts of the filaments are found on thrombolitic microbialites. These microbialites are up to a meter tall
and are located the intertidal region of the back reef of an
algal-ridge fringing reef complex that extends for 2.5 km
along the eastern shore of the Pleistocene island Highborne
Cay (Fig. 1). Sampled thrombolitic microbialites are located
at Highborne Cay Sites 6 and 8 of Andres & Reid (2006).
Several of the thromboltic microbialites were found growing
on top of 1084-year-old vermetid-gastropod shells, indicating
recent growth (Planavsky and Reid, unpublished data). This
age is based on radiometric (14C) dating performed on
cleaned shell fragments using Accelerator Mass Spectrometry
at Beta Analytical, Miami, Florida.
The Highborne Cay fringing reef complex contains
well-laminated stromatolites, in addition to the thrombolitic
microbialites (Reid et al., 1999, 2000). The stromatolites are
also best developed in the back-reef setting. The reef is a
highly dynamic system, and all of the microbialites are periodically covered by carbonate sand (Andres & Reid, 2006).
Continuous monitoring of the Highborne reef complex
for over 2 years (2005–2006) indicates that there are periods when eukaryotes – rather than cayanobacteria – are the
dominant photosynthetic organisms on the surfaces of
thromboltic microbialites. The eukaryotes include green
algae, red algae, and a pink layer rich in EPS and spherical
spores, which have not received proper taxonomic treatment
(see Littler et al., 2005, for discussion of Highborne Cay
algae). Micritic aragonite precipitates in the pink layer forming crude laminations at the top of nearshore buildups (Reid
et al., 1999). Except for these micritic laminations, the
thrombolitic microbialites have clotted and mottled fabrics
(Fig. 2) (Reid et al., 1999).
MATERIALS AND METHODS
Cyanobacterial mats were examined within an hour of collection using light and fluorescence microscopy. The fluorescence microscope (using a 490-nm excitation filter) was used
to visualize carbonate precipitates and examine the degree of
cyanobacterial autoflorescence. Cyanobacterial fluorescence,
as viewed with the 490-nm excitation filter, is caused by
accessory photosynthetic pigments – predominately phycobiliproteins – and can thus be used to estimate photosynthetic
ability.
Clusters of cyanobacterial cells were fixed in 4.5% gultaraldhyde in sodium cacodylate buffered solution within an
hour of collection for electron microscopy work. We did a
568
N. PLANAVSKY et al.
Fig. 1 Study location. (A) Map of study area, showing the location of the Highborne Cay reef system. The reef system is located at the interface of open ocean waters
to the east and Bahama Bank to the west. (B) Photo of the thrombolitic microbialites during a period of low tide. (C) Ariel photos of the Highborne Cay reef system.
The examined thrombolitic microbialites are located in the backreef setting at Sites 6 and 8.
post-fixation with osmium tetroxide, within a week of the
initial fixation. Material used for electron microcopy was
coated in palladium and viewed using a FEI ⁄ Philips XL30
environmental scanning electron microscope (E-SEM) with
an Oxford L300Qi-Link ISIS EDS at University of Miami,
Department of Geology.
Our observations on the early diagenetic history of calcified
cyanobacteria are from 42 standard petrographic thin sections. All material was embedded under vacuum with epoxy
prior to sectioning. Nineteen of these thin sections come from
two complete thrombolitic microbialites excavated from
Highborne Cay (Site 6 of Andres & Reid, 2006). The remaining thin sections are from the upper, surficial sections of
Highborne Cay thrombolitic microbialites.
We extracted calcified, autofluorescent cyanobacteria cells
for carbonate carbon and oxygen isotopic analysis. The
calcified filaments were isolated from surrounding sediment at
50· magnification using a dissecting microscope. The purity
of a subset of the calcified filament samples was checked using
scanning electron microscopy (SEM). All samples examined
using SEM contained minor amounts of sediment impurities.
The isotopic values, therefore, are a qualitative, rather than
truly quantitative, estimate of the calcified filament isotopic
values.
Carbonates were isotopically analyzed with a Kiel III
automated carbonate device interfaced to a Thermo Finnigan
Delta-plus stable isotope ratio mass spectrometer at the Stable
Isotope Laboratory at the Rosenstiel School of Marine and
Atmospheric Science, Miami Fl. Results were corrected for
standard drift and isobaric interferences and are expressed
relative to Vienna Peedee belemnite. Instrument precision
was better than 0.15& for d18O and d13C (2r).
2009 Blackwell Publishing Ltd
Modern marine calcified cyanobacteria
569
Fig. 2 Photos of cut thrombolitic microbialites. (A) Microbialite from the distal
section of the backreef in Highborne Cay Site 6. Slab is 1 m across. (B) Microbialite from the near-shore section of the backreef in Highborne Cay Site 6. Slab
is 1.5 m across. Both microbialites lack prominent laminations, contain
abundant voids, and have a weakly clotted fabric.
The carbonate mineralogy of filaments was determined
using X-ray diffraction with a PAN alytical X’Pert X-ray
diffractometer operated at the Stable Isotope Laboratory of
the Rosenstiel School of Marine and Atmospheric Sciences.
Similar to the isotopic work, calcified, autofluorescent cyanobacteria cells were isolated from surrounding sediment using a
dissecting microscope. Additionally, using electron dispersive
spectroscopy (EDS) we were able to determine carbonate
mineralogy at the micron scale (see Planavsky & Ginsburg,
2009, for information about determining mineralogy with
EDS).
RESULTS
Description of calcified filaments
Calcified cyanobacteria filaments, along with trapped and
bound sand grains, form unlaminated tuffs or buttons that
cover the tops and sides of the thrombolitic microbialites. The
tuffs are typically between 1 and 5 cm across and many are
exposed at low tide (Fig. 3A). A single variety of cyanobacteria, Dichothrix, form the calcified filaments that define the
unlaminated tuffs on the Highborne Cay thrombolitic structures. We identified the filaments as Dichothrix based on the
presence of common lateral false branching, with the branch
first running parallel to the original trichome, as well as the
2009 Blackwell Publishing Ltd
Fig. 3 Photos of the calcified cyanobacterial filaments. (A) Photo of a tuft of
vertically oriented calcified Dichothrix filaments from the surface of a thrombolitic microbialites. Scale bar is 1 cm. (B) Photo showing the carbonate coating on
Dichothrix filaments. Scale 1 mm.
presence of basal heterocytes, obligatory sheaths, narrowing
apical ends, and a lack of akinetes. All observed Dichothrix filaments have some degree of calcification, but the initial calcification was rarely observed to complete coat the filaments.
Other cyanobacteria can be present within the tuffs, including
cyanobacteria in genus Oscillatoria. The Oscillatoria, in contrast to the Dichothrix filaments, do not show well-defined
mucilaginous sheaths. Although, the tuffs are dominated by
vertically oriented cyanobacteria (Fig. 3A), occasional red
algae may be interspersed, especially on the tops upper
surfaces of the more seaward microbialites. No carbonate
precipitates were observed on the red algae or the adjacent
sediment.
Initial calcification occurs around Dichothrix filaments that
lack obvious signs of filament or sheath degradation (Figs 4A
and 5A). Surficial calcifying filaments are strongly autofluorescence (viewed with 490-nm excitation filter). The degree of
autofluorescence in the Dichothrix cell decreases markedly
over a centimeter scale with depth in the filament tufts
(Fig. 4B). The initial carbonate precipitation occurs in the
570
N. PLANAVSKY et al.
Fig. 4 Light micrographs of calcified Dichothrix filaments under florescent
light with a 490-nm excitation filter. The carbonate and photosynthetic pigment
are fluorescing blue and orange, respectively. (A) Micrograph of a Dichothrix
filament from the surficial section of a tuft of filaments. The cell shows strong
autofluorescence, indicating photosynthetic ability. (B) Micrograph of a
Dichothrix filament from the basal section of a tuft of filaments. The cell does
not display autofluorescence and contains unevenly distributed carbonate
precipitates in the cell’s sheath. Scale bars 20 lm.
exopolymeric sheath surrounding the cyanobacterial cell
(Fig. 5A). The initial carbonate precipitates are randomly
oriented fine-grained (submicron to 50 lm crystals) acicular
aragonite (Figs 6A and 7A).
The distinct calcified filaments present on the uppermost
section of the microbialite grade gradually downward from the
surface into poorly defined, degraded calcified cells and associated fine-grained, micrite precipitates (Fig. 5). The mucilaginous sheaths in degraded cyanobacterial cells are typically
absent or non-continous (Figs 5B and 6B). Carbonate precipitates on filaments with signs of degradation are sporadic, and
the aragonite crystals exhibit fused and indistinct crystal faces
(Fig. 7B). These crystal features are similar to those observed
in other organic-rich modern carbonates that have experienced penecontemporaneous aragonite recrystallization
(Macintyre & Reid, 1995; Reid & MacIntyre, 1998). The
poorly defined cells and associated precipitates grade into a
fabric that lacks distinguishable remnants of cyanobacterial
cells (Fig. 5C). The amount of intergranular carbonate precipitate increases during the transition from distinct calcified cells
surrounded by sand grains into well-cemented sand lacking
distinct calcified cyanobacteria (Fig. 5C). We observe this diagenetic progression – from well-defined calcified cyanobacterial
cells to abundant micritic cements – over a depth range of a
several centimeters. Calcified cyanobacteria were not observed
lower than 6.5 cm below the microbial mat-water interface.
The lower, older sections of the thromboltic microbialites
at depths of 10 cm to 1 m contain abundant submarine
precipitates. These precipitates are typically micritic, although
fibrous aragonite cement is locally abundant. The lower
sections of the microbialites are also heavily bored and locally
contain abundant encrusting foraminifera. Extensive micritization is common. In some cases, the tuffs of calcified
filaments are growing on a distinct micritization front.
Fig. 5 (A–C) Light micrographs illustrating the early diagenetic transition from
distinct calcified cyanobacterial filaments to patchy fine-grained carbonate
cements. The light micrographs in A–C are taken from a single microbialite over
a 7-cm vertical distance. Calcified filaments are also absent from more basal
sections of the microbialite indicating that the calcified cyanobacterial microfossils would not be preserved in the geological record. Scale bars 100 lm.
2009 Blackwell Publishing Ltd
Modern marine calcified cyanobacteria
571
Fig. 8 Carbon and oxygen isotope values of filament precipitates ( ),
stromatolite fine-grained precipitates (·), bulk unlaminated microbialites, (s),
and Highborne Cay ooids ()). Stromatolite data from Andres et al. (2006).
the bulk thrombolitic microbialites, and the precipitates from
the adjacent stromatolites.
Carbonate oxygen isotopes values from the calcified
filaments, with limited exceptions, are 0 ± 0.5&, similar to
the Highborne Cay sediments, the bulk thrombolitic microbialites, and the precipitates from the adjacent stromatolites
(Andres et al., 2006). Three samples of calcified filaments
display d18O values £+1& (Fig. 8).
Fig. 6 SEMs of calcified filaments. (A) SEM showing fine-grained carbonate
precipitate within the mucilaginous sheath (S) surrounding the cyanobacteria
cell ⁄ trichome (T). (B) SEM of a calcified filament that has undergone degradation. The carbonate precipitates in the degraded cyanobacteria sheath (S) are
more sporadic than in the well-preserved sheath shown in plate A. Scale bars
10 lm.
Stable isotope results
Carbonate from the calcified filaments has d13C isotope values
ranging from +4.50& to +5.82& (Fig. 8). Detrital carbonate
grains and fine-grained precipitates from the adjacent stromatolites at Highborne Cay have a range of d13C values from
+4.61& to +4.83& and +3.1& to +4.58& respectively
(Andres et al., 2006). Bulk samples of the unlaminated microbialites have carbonate d13C values that range from +4.3% to
+4.79& (Fig. 8). The d13C values of the calcified filaments
are significantly higher than the Highborne Cay sediments,
DISCUSSION
Formation of calcified cyanobacteria
Several lines of evidence from the present study indicate
in vivo cyanobacterial calcification in a normal salinity,
modern marine environment. Calcification is occurring in the
uppermost section of the Dichothrix tufts, where there are
high rates of photosynthesis indicating an active cyanobacterial community (Myshrall et al., 2008). The presence of some
degree of sheath calcification in all of the observed Dichothrix
filaments provides strong support for calcification occurring
during the cyanobacterial life cycle. Strong autofluorescence
in surficial calcified cells likely indicates photosynthetic ability.
The lack of obvious signs of heterotrophic degradation in the
initial calcified cells also provides support for in vivo calcification (Fig. 9).
Fig. 7 SEMs of carbonate from calcified filaments. (A) SEM of initial carbonate precipitates in the mucilaginous sheath of a Dichothrix filament. The carbonate is
composed of acicular aragonite needles with distinct crystal faces (B) SEM of carbonate precipitates in the mucilaginous sheath of a Dichothrix filament that has
undergone degradation. The carbonate crystals are indistinct and contain fused crystal faces, which indicate early digenetic dissolution–reprecipitation reactions. Scale
bars 5 lm.
2009 Blackwell Publishing Ltd
572
N. PLANAVSKY et al.
Fig. 9 Schematic showing the stages of formation
and degradation of calcified cyanobacterial filaments in Highborne Cay microbialites. See text for
further details.
The presence in vivo calcification within the Dichothrix
sheath is consistent with photosynthesis-induced carbonate
precipitation: cyanobacterial sheaths experience a significant
increase in pH during photosynthesis due to carbon dioxide
uptake (Visscher & van Gemerden, 1991; Arp et al., 2001).
Carbon dioxide degassing is not inducing carbonate precipitation within the Dichothrix tufts. The lack of carbonate
precipitation on the red algae interspersed with the calcifying
filaments or the adjacent sediment is inconsistent with carbon
dioxide degassing driving carbonate precipitation. Dichothrix
filaments are calcifying on the sides of microbialites that are
unaffected by exposure. Further, oxygen isotopes from the
carbonate precipitates from Dichothrix sheaths, with limited
exception, do not show an evaporative signal (carbonate with
high d18O values). An evaporative signal would likely be
present if carbon dioxide degassing linked with elevated
temperatures had driven calcification. However, carbon dioxide degassing can also be caused by increased agitation, which
would not result in an evaporative signature in carbonate
oxygen isotope values.
The carbonate d13C isotope values from Highborne Cay
microbialites provide additional insights into the mechanisms
driving calcium carbonate precipitation. Significantly more
positive d13C isotope values in the calcified filaments than in
the adjacent stromatolite precipitates indicate that the mode
of calcification is distinctly different in each microbialite type.
The micritic laminations in the Highborne Cay stromatolites
precipitate in a zone of localized, intense sulfate reduction
(Visscher et al., 2000). This correlation was shown through
silver-foil experiments in the microbial ecosystems forming
the stromatolites, which track microbial sulfide production
from sulfate (Visscher et al., 2000). The stromatolite precipitates contain carbon isotope values that are lower than would
be predicted if precipitation occurred from the ambient
dissolved inorganic carbon (DIC) reservoir (Andres et al.,
2006). The light d13C isotope values are likely due to precipitation in an environment with bicarbonate derived from isotopically light organic matter remineralization (Andres et al.,
2006).
Significantly more positive d13C values in the calcified filaments of the thrombolitic microbialites – compared to
those in the adjacent stromatolite precipitates or the surrounding sediment – suggests carbonate precipitation in the
sheath of these filaments was in part photosynthetically
induced. During cyanobacterial photosynthesis, preferential
uptake of 12C-enriched carbon dioxide or bicarbonate creates
a 13C-enriched microenvironment with an elevated pH in the
mucilaginous sheath (for review see Riding, 2000, 2006).
Since the calcified filaments analyzed isotopically contained
minor amounts of contaminating carbonate sediment, the
2009 Blackwell Publishing Ltd
Modern marine calcified cyanobacteria
carbonate d13C values cannot be used to quantitatively resolve
DIC reservoir shifts. Highborne Cay sediments have significantly lower d13C values than the calcified filament precipitates, indicating the true values of these precipitates are
slightly higher than reported.
Dichothrix filaments have a different calcification history
than the Schizothrix filaments in adjacent stromatolites. Initial
calcification in Dichothrix is occurring in vivo and photosynthetic activity appears to be one of the processes inducing
calcification. There is no evidence for in vivo calcification of
Schizothrix filaments (Reid et al., 2000; Visscher et al., 2000;
Andres et al., 2006). However, this does not support that
initial Dichothrix calcification is a strictly photosynthetically
induced process. In previous work, higher rates of heterotrophic activity were found in sections of Bahamian microbial mats
with living, highly productive cyanobacteria than in sections
with decaying cyanobacteria (including heterotrophic metabolisms likely to induce carbonate precipitation like sulfate reduction) (Visscher et al., 2000; Braissant et al., 2009). Therefore,
it is likely that the initial carbonate precipitates in the Dichothrix
sheath are linked with both heterotrophic and photosynthetic
activity. This interpretation is consistent with the presence of
distinct but small differences in carbon isotope values between
the likely heterotrophically induced stromatolite precipitates
and the Dichothrix sheath precipitates. Further, more microbiologically oriented research will be required to elucidate the
relative importance of heterotrophic and photosynthetic
activity in causing the initial Dichothrix filament calcification.
The absence of filament calcification in cyanobacteria other
than Dichothrix at Highborne Cay may be linked with differences in EPS composition, since EPS has been shown to have
a strong influence on the style and extent of microbial calcification (e.g. Braissant et al., 2007; Dupraz et al., in press).
The EPS of the sheathed cyanobacteria Schizothrix, the
dominant cyanobacteria in the stromatolites at Highborne
Cay, initially has a strong inhibitory effect on carbonate
precipitation (Kawaguchi & Decho, 2002). It is possible that
the EPS produced by Dichotrix has less pronounced inhibitory
effect on calcification (e.g. through a reduced Ca-binding
capacity compared to other cyanobacterial EPS), allowing for
sheath calcification. Alternatively, the local production of EPS
by Dichotrix could be in balance with degradation by heterotrophic bacteria, effectively reducing the cation-binding
potential. Furthermore, if the dense clusters of cyanobacteria
in the thrombolites locally have very high rates of photosynthesis, this will result in a pH increase, as is typically observed
in microbial mats (Revsbech & Jørgensen, 1986; Visscher
et al., 1991). The elevated pH not only favors chemical conditions for precipitation, it also causes the EPS to form gels
(Sutherland, 2001) potentially eliminating inhibition of carbonate precipitation. The different calcification mechanisms
at Highborne Cay clearly indicate that benthic microbial communities can have a strong control on the type of microbial
carbonate precipitation.
2009 Blackwell Publishing Ltd
573
The Highborne Cay thrombolitic microbialites demonstrate that penecontemporaneous diagenesis can have a strong
influence on microbial carbonate fabrics. Abundant carbonate
precipitation occurs after the initial, in vivo calcification that
forms the calcified filaments. The loss of the distinct shape of
the calcified cells suggests that there is localized carbonate
dissolution as well as precipitation of secondary carbonate
cements during early diagenesis (Fig. 9). The fine-scale
microstructures in the calcified filaments provide additional
evidence for carbonate dissolution. The fused and indistinct
aragonite crystals present in the Dichotrix sheaths that have
undergone structural degradation are indicative of multiple
stages of aragonite dissolution and reprecipitation (Macintyre
& Reid, 1995; Reid & MacIntyre, 1998). This altered aragonite fabric is a contrast to that present in calcified filaments
that have undergone little structural degradation, where
aragonite crystals are acicular and distinct. Localized dissolution–reprecipitation is common in a wide range of modern
shallow marine carbonates (Reid & MacIntyre, 1998) including subtidal Bahamian microbialites (Planavsky & Ginsburg,
2009). Carbonate under-saturation is likely induced by a combination of sulfide production during initial stages of sulfate
reduction, sulfide oxidation, and aerobic respiration (Morse
& MacKenzie, 1990; Walter et al., 1993; Visscher et al.,
1998; Dupraz & Visscher, 2005; Visscher & Stolz, 2005; Hu
& Burdige, 2007).
Temporal distribution and abundance of calcified
cyanobacteria
Our study offers insights into the factors controlling the temporal distribution of calcified cyanobacteria microfossils
(Fig. 10). The rarity of these microfossils since the early Cretaceous (around 145 Ma) (Fig. 10A) has been linked with
inhibited fossil formation due to low Ca concentrations (and
hence a lower calcium carbonate saturation state) (Arp et al.,
2001). Calcium concentration drawdown was linked with the
radiation of planktonic calcareous algae such as coccoliths
(Arp et al., 2001). This model of ocean chemistry is at odds
with modeling work on Phanerozoic cation concentrations,
which suggest that the Cretaceous contained the highest Ca2+
concentrations in the Phanerozoic (Fig. 10B) (Hardie, 1996;
Lowenstein et al., 2001). The model of Hardie (1996) does
not take into account the effects planktonic calcareous algae
radiation (Arp et al., 2001), but (based on carbonate petrology) the early Cretaceous appears to be a ‘calcite sea’ time
period (e.g. Sandberg, 1983), which is consistent with high
Ca2+ concentrations (Lowenstein et al., 2001). Coccolith
radiation is also inferred to have lowered the global marine
carbonate saturation state by decreasing the carbonate ion
concentrations, which – again – may have decreased the ability
of cyanobacteria to from calcified microfossils (Riding, 2000).
However, the widespread occurrence of calcifying cyanobacterial filaments in several modern marine localities reveals that
574
N. PLANAVSKY et al.
Fig. 10 (A) Reported occurrences of calcified cyanobacteria microfossils per
10 Ma through the Phanerozoic (from Arp et al., 2001). (B) Model-based (solid
black line; Stanley and Hardie, 1998) and fluid inclusion-based (vertical gray
squares; Horita et al., 2002) estimates of Ca concentration throughout the
Phanerozoic. (C) Model of surface calcite saturation state through the Phanerozoic in an ocean with deep-sea carbonate burial caused by a rain of calcified
planktonic organisms (lower black line) and in an ocean with carbonate production occurring exclusively on shelf environments (upper black line) (from
Ridgwell, 2005). The formation and early diagenetic destruction of calcified filaments in the modern oceans suggests that the low abundance of calcified
cyanobacterial microfossils over last 150 Ma and from 250 to 300 Ma may be
the results of low preservation potential as well as inhibited microfossil formation due to low calcium or carbonate ion concentrations.
precursors to these microfossils can form in modern oceans.
Besides Highborne Cay, calcified filaments are common in the
reef tract off Stocking Island (eastern Bahamas) (MacIntyre
et al., 1996) in carbonate sands on the eastern Bahama Bank
(Winland & Matthews, 1974) in peritidal environments off
Andros Island (western Bahamas) (Hardie, 1977), and in
pools on Aldabra Atoll (Seychelles) (Riding, 1977). Their
presence is significant since modern oceans are inferred to
contain some of the lowest marine Ca2+ concentrations
(Hardie, 1996; Lowenstein et al., 2001) and have close to the
lowest levels of carbonate supersaturation (Ridgwell, 2005;
Ridgwell & Zeebe, 2005) in the Phanerozoic (Fig. 10B). The
limited number of occurrences of calcified filaments in the
modern oceans, however, demonstrates that cyanobacteria
filament calcification is not a ubiquitous process.
The destruction of the Highborne Cay cyanobacterial
microfossils during early diagenesis suggests that preservation
potential could exert a strong control on the abundance of the
calcified cyanobacteria in the fossil record. The shift to
widespread carbonate production by pelagic organisms
dramatically altered the carbon cycle by shifting the dominant
carbonate sink from shallow to deep-sea environments (Ridgwell, 2005; Ridgwell & Zeebe, 2005). Geochemical box
models of atmosphere-ocean-sediment carbon cycling suggest
that this transformation caused a sharp drop in the calcium
carbonate saturation states and decreased the size of the DIC
reservoir (Ridgwell, 2005) (Fig. 10C). These decreases would
have resulted in a marked decline in the acid buffering capacity
of seawater, increasing the importance of carbonate dissolution during early diagenesis. We propose that the rarity of
cyanobacterial calcimicrofossils since the early Cretaceous is
linked in part with this restructuring of the carbon cycle and
the corresponding increase in potential for destruction of
cyanobacterial microfossils during early diagenesis.
The limited abundance of calcified cyanobacteria microfossils in the Permian (Arp et al., 2001) may also be partially
caused by low preservation potential. The Permian was a time
of non-skeletal aragonite or high Mg-calcite (e.g. Sandberg,
1983; Lowenstein et al., 2001) and metastable aragonite and
high Mg-calcite will be more severely altered during early
diagenesis than low Mg-calcite. However, the Triassic is also
time of an ‘aragonite sea’ and contains notably more reported
occurrences of calcified cyanobacteria than in the Permian. It
is likely, therefore, that inhibited formation of calcified
cyanobacteria and possibly rock abundance biases are also significant factors controlling the number of occurrences ⁄
abundance of calcified cyanobacterial microfossils in the Phanerozoic.
The abundance of calcified filaments in the late Jurassic
(Fig. 10A) indicates an interval of high preservation and
calcifying potential. This is at odds with models that suggest
that the restructuring of the carbon cycle to a system with predominately deep-sea carbonate deposition occurred by this
time. As discussed above, the shift to a deep-sea-dominated
carbonate cycle would have likely greatly decreased the preservation and calcifying potential of calcified cyanobacteria.
Therefore, although there was a large increase in diversity and
abundance of calcifying pelagic organisms in the Jurassic
(Martin, 1995), it appears they did not become abundant
enough to revolutionize the carbon cycle until the Cretaceous. This is in accordance with sedimentological evidence
that suggests deep-sea carbonate burial increased throughout
the Mesozoic and reached it zenith during the Cretaceous
(Siesser, 1993). Thus, the record of calcified cyanobacteria
provides insights into the timing of one of the major transitions in Earth’s history and biosphere that is difficult to gauge
through traditional proxies, such as the diversity of calcifying
pelagic organisms (Martin, 1995) or the percent of ophilite
complexes containing carbonate (Boss & Wilkinson, 1991).
2009 Blackwell Publishing Ltd
Modern marine calcified cyanobacteria
These traditional proxies for pelagic carbonate production are
only weakly linked to amount of carbonate deposition.
CONCLUSIONS
We documented the formation and early diagenetic history
of calcified cyanobacteria from a modern open marine setting
at Highborne Cay, Bahamas. A single variety of cyanobacteria
at Highborne Cay, identified as Dichothrix sp., produce the
calcified filaments. Calcification initially occurs in vivo within
the cyanobacterial sheath. The calcified filaments have significantly more positive carbonate d13C isotope values than
precipitates from adjacent stromatolites or than the surrounding sediment. These isotopic values suggest photosynthetic
activity was the central process driving carbonate precipitation
in the sheaths of Dichothrix cells. Variation in the calcification
styles of Highborne Cay benthic ecosystems [e.g. formation
of well-laminated stromatolites versus (non-laminated)
thrombolitic microbialites] clearly indicates that there can be a
strong ecosystem control on microbial calcification.
During early diagenesis, the calcified filaments are degraded
and there is abundant carbonate precipitation. The lack of
preservation of the Highborne Cay calcified filaments suggests
that the absence of calcified cyanobacteria from periods in the
Phanerozoic does not necessarily imply inhibited formation.
Poor preservation potential is likely a factor responsible for the
lack of marine calcified cyanobacterial fossils over the past
65 Myr as well as inhibited formation.
ACKNOWLEDGEMENTS
NP received support from the Ocean and Research and Education Fund. RPR acknowledges support from NSF grant EAR
0221796 and TWL from the NASA Exobiology program.
KLM received funding from the Paleontological Society
Grant-In-Aid program and from the Geological Society of
America Graduate Student Research Fund. PTV acknowledges
support from NASA JRI through the Ames Research Center.
NP is greatly indebted to Robert Ginsburg for discussion and
guidance. The manuscript was improved due to insightful comments from three anonymous reviewers and Lee Kump and
benefited from discussions with Noel James, Guy Narbonne,
and Mark Palmer. This is RIBS Contribution #58.
REFERENCES
Andres MS, Reid RP (2006) Growth morphologies of modern marine
stromatolites: a case study from Highborne Cay, Bahamas.
Sedimentary Geology 185, 319–328.
Andres MS, Sumner DY, Reid RP, Swart PK (2006) Isotopic fingerprints of microbial respiration in aragonite from Bahamian stromatolites. Geology 34, 973–976.
Arp G, Reimer A, Reitner J (2001) Photosynthesis-induced biofilm
calcification and calcium concentrations in Phanerozoic oceans.
Science 292, 1701–1704.
2009 Blackwell Publishing Ltd
575
Arp G, Reimer A, Reitner J (2003) Microbialite formation in seawater
of increased alkalinity, Satonda Crater Lake, Indonesia. Journal of
Sedimentary Research 73, 105–117.
Boss SK, Wilkinson BH (1991) Planktogenic eustatic control on cratonic
oceanic carbonate accumulation. Journal of Geology 99, 497–513.
Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher
PT (2007) Exopolymeric substances of sulfate-reducing bacteria:
interactions with calcium at alkaline pH and implications for formation of carbonate minerals. Geobiology 5, 401–411.
Braissant O, Decho AW, Przekop KM, Gallagher KL, Glunk C,
Dupraz C, Visscher PT (2009) Characteristics and turnover of exopolymeric substances in a hypersaline microbial mat. FEMS Microbiology Ecology 67, 293–307.
Decho AW (2000) Exopolymer-mediated microdomains as a
structuring agent for microbial activities. In Microbial Sediments
(eds Riding R, Awramik SM). Springer-Verlag, Berlin, pp.
9–15.
Dupraz CD, Visscher PT (2005) Microbial lithification in marine
stromatolites and hypersaline mats. TRENDS in Microbiology 13,
429–438.
Dupraz CD, Reid PR, Braissant O, Decho AW, Norman SR, Visscher
PT (in press) Processes of carbonate precipitation in modern microbial mats. Earth-Science Reviews.
Hardie LA, ed. (1977) Sedimentation on the modern carbonate tidal
flats of northwest Andros Island, Bahamas. Johns Hopkins
University Studies in Geology 22, 202.
Hardie LA (1996) Secular variation in seawater chemistry: an explanation for the coupled secular variation in the mineralogies of marine
limestones and potash evaporites over the past 600 my. Geology 24,
279–283.
Horita J, Heide Zimmermann H, Holland HD (2007) Chemical
evolution of seawater during the Phanerozoic: implications from
the record of marine evaporates. Geochimica et Cosmochimica Acta
66, 3733–3756.
Hu XP, Burdige DJ (2007) Enriched stable carbon isotopes in the
pore waters of carbonate sediments dominated by seagrasses:
evidence for coupled carbonate dissolution and reprecipitation.
Geochimica et Cosmochimica Acta 71, 129–144.
Kah LC, Riding R (2007) Mesoproterozoic carbon dioxide levels
inferred from calcified cyanobacteria. Geology 35, 799–802.
Kawaguchi T, Decho AW (2002) Isolation and biochemical characterization of extracellular polymeric secretions (EPS) from modern
soft marine stromatolites (Bahamas) and its inhibitory effect on
CaCO3 precipitation. Preparative Biochemistry & Biotechnology
32, 51–63.
Knoll AH, Fairchild IJ, Swett K (1993) Calcified microbes in Neoproterozoic carbonates – implications for our understanding of the
Proterozoic Cambrian transition. Palaios 8, 512–525.
Littler DS, Littler MM, Macintyre IG, Bowlin E, Andres MS, Reid RP
(2005) Guide to the dominant macroalgae of the stromatolite
fringing reef complex, Highborne Cay, Bahamas. Atoll Research
Bulletin 532, 67–92.
Lowenstein TK, Timofeeff MN, Brennan ST, Hardie LA, Demicco
RV (2001) Oscillations in Phanerozoic seawater chemistry:
evidence from fluid inclusions. Science 294, 1086–1088.
Macintyre IG, Reid RP (1995) Crystal alteration in a living calcareous
alga (Halimeda) – implications for studies in skeletal diagenesis.
Journal of Sedimentary Research 65, 143–153.
MacIntyre IG, Reid PR, Stenck RS (1996) Growth history of stromatolites in a Holocene fringing reef, Stocking Island, Bahamas.
Journal of Sedimentary Research 66, 231–242.
Martin RE (1995) Cyclic and secular variation in microfossil biomineralization – clues to the biogeochemical evolution of Phanerozoic
oceans. Global and Planetary Change 11, 1–23.
576
N. PLANAVSKY et al.
Merz MUE (1992) The biology of carbonate precipitation by
cyanobacteria. Facies 26, 81–101.
Morse J, MacKenzie F (1990) Geochemistry of Sedimentary
Carbonates. Elsevier, Amsterdam.
Myshrall KL, Norman RS, Thompson JB, Visscher PT (2008) Microbial community composition in modern thrombolites: a comparison of open marine and freshwater systems using molecular
techniques. Geological Society of America Abstracts with Programs
40, 412.
Planavsky N, Ginsburg RN (2009) Thaponomy of modern marine
Bahamian microbialites. Palaios 24, 5–24.
Reid RP, MacIntyre IG (1998) Carbonate recrystallization in shallow
marine environments: a widespread diagenetic process forming
micritized grains. Journal of Sedimentary Research 68,
928–946.
Reid RP, Macintyre IG, Steneck R (1999) A microbialite ⁄ algal ridge
fringing reef complex, Highborne Cay, Bahamas. Atoll Research
Bulletin 466, 1–18.
Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C,
Macintyre IG, Paerl HW, Pinckney JL, Prufert-Bebout L, Steppe
TF, DesMarais DJ (2000) The role of microbes in accretion, lamination and early lithification of modern marine stromatolites.
Nature 406, 989–992.
Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use in
microbial ecology. Advances in Microbial Ecology 9, 293–352.
Ridgwell A (2005) A mid Mesozoic revolution in the regulation of
ocean chemistry. Marine Geology 217, 339–357.
Ridgwell A, Zeebe RE (2005) The role of the global carbonate cycle
in the regulation and evolution of the Earth system. Earth and
Planetary Science Letters 234, 299–315.
Riding R (1977) Calcified Plectonema (blue-green algae), a recent
example of Girvanella from Aldabra Atoll. Palaeontology 20, 33–46.
Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47, 179–214.
Riding R (2006) Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4, 299–316.
Riding R, Liang LY (2005) Geobiology of microbial carbonates:
metazoan and seawater saturation state influences on secular trends
during the Phanerozoic. Palaeogeography Palaeoclimatology
Palaeoecology 219, 101–115.
Sandberg PA (1983) An oscillating trend in Phanerozoic non-skeletal
mineralogy. Nature 305, 19–22.
Siesser W (1993) Calcareous nannoplankton. In Fossil Prokaryotes and
Protists (ed. Lipps J). Blackwell Scientific, Oxford, pp. 169–201.
Stanley SM, Hardie LA (1998) Secular oscillations in the carbonate
mineralogy of reef-building and sediment-producing organisms
driven by tectonically forced shifts in seawater chemistry. Palaeogeography, Palaeoclimatology, Palaeoecology 144, 3–19.
Sumner DY, Grotzinger JP (1996) Were kinetics of Archean calcium
carbonate precipitation related to oxygen concentration? Geology
24, 119–122.
Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky
framework. Microbiology 147, 3–9.
Turner EC, James NP, Narbonne GM (2000) Taphonomic control
on microstructure in early neoproterozoic reefal stromatolites and
thrombolites. Palaios 15, 87–111.
Visscher PT, Stolz JF (2005) Microbial mats as bioreactors: populations, processes, and products. Palaeogeography, Palaeoclimatology,
Palaeoecology 219, 87–100.
Visscher PT, van Gemerden H (1991) Production and consumption
of dimethyl-sulfoniopropionate in marine microbial mats. Applied
and Environmental Microbiology 57, 3237–3242.
Visscher PT, Quist P, van Gemerden H (1991) Methylated sulfur
compounds in microbial mats: in situ concentrations and metabolism by a colorless sulfur bacterium. Applied and Environmental
Microbiology 57, 1758–1763.
Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG, Thompson J Jr (1998) Formation of lithified micritic laminae in modern
marine stromatolites (Bahamas): the role of sulfur cycling.
American Mineralogist 83, 1482–1491.
Visscher PT, Reid RP, Bebout BM (2000) Microscale observations of
sulfate reduction: correlation of microbial activity with lithified
micritic laminae in modern marine stromatolites. Geology 28,
919–922.
Walter MR, Heys GR (1985) Links between the rise of the metazoa
and the decline of stromatolites. Precambrian Research 29,
149–174.
Walter LM, Bischof SA, Patterson WP, Lyons TW (1993) Dissolution
and recrystallization in modern shelf carbonates – evidence from
pore-water and solid-phase chemistry. Philosophical Transactions of
the Royal Society of London, Series A 344, 27–36.
Winland HD, Matthews RK (1974) Origin and significance of grapestone, Bahama Islands. Journal of Sedimentary Petrology 44,
921–927.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article:
Table S1 Stable isotope values and sample identification for data shown in
main text Fig. 8.
Please note: Wiley-Blackwell is not responsible for the content
or functionality of any supporting materials supplied by the
authors. Any queries (other than missing material) should be
directed to the corresponding author for the article.
2009 Blackwell Publishing Ltd