formationanddiagenesisofmodernmarinecalciﬁed...

Formation and diagenesis of modern marine calcifiedcyanobacteriaN. PLANAVSKY,1 ,2 R. P. REID,1 T. W. LYONS,2 K. L. MYSHRALL3 AND P. T. VISSCHER3

1Rosenstiel School of Marine andAtmospheric Sciences, Miami, FL, USA2Department of Earth Sciences, University of California, Riverside, Riverside, CA, USA3Department of Marine Sciences, University of Connecticut, Groton, CT, USA

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 cyano-

bacteria 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, indi-

cating there can be a strong taxonomic control over the mechanism of microbial calcification. Petrographic anal-

yses 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 compo-

nent of marine carbonate reefs and sediments deposited from

550 to 100 Ma (Riding, 2000; Arp et al., 2001). Calcified-microfossils morphologies are diverse, and many have been

assigned formal taxonomic names (Riding, 2000). Filamen-

tous taxa, such Girvanella are likely the most common calci-

fied 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 Creta-

ceous (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 dramati-

cally different from those of marine settings, these modern

calcified cyanobacteria are not direct analogs for ancient

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 ulti-

mately caused by a local increase in calcium carbonate satura-

tion 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., inpress). Uptake of carbon dioxide during cyanobacterial

photosynthesis increases the pH surrounding the cyanobacte-

rial cell, which favors carbonate precipitation. Bicarbonate is

! 2009 Blackwell Publishing Ltd 1

Geobiology (2009), 7, 1–11 DOI: 10.1111/j.1472-4669.2009.00216.x

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 typi-

cally 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) pro-

duced 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 pro-

cesses, large amounts of Ca2+ ions are released, promoting cal-

cification (Dupraz & Visscher, 2005).

The factors controlling the temporal distribution of calci-

fied 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 micro-

fossil 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 modernmarine calcify-

ing 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

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 (76"49¢W, 24"43¢N)

Exuma, Bahamas. Tufts of the filaments are found on throm-

bolitic 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 themicrobialites are periodi-

cally covered by carbonate sand (Andres & Reid, 2006).

Continuous monitoring of the Highborne reef complex

for over 2 years (2005–2006) indicates that there are peri-

ods 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 form-

ing 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 collec-

tion using light and fluorescence microscopy. The fluores-

cence 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 phyco-

biliproteins – and can thus be used to estimate photosynthetic

ability.

Clusters of cyanobacterial cells were fixed in 4.5% gultarald-

hyde in sodium cacodylate buffered solution within an

hour of collection for electron microscopy work. We did a

2 N. PLANAVSKY et al.

! 2009 Blackwell Publishing Ltd

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 sec-

tions. 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 remain-

ing 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).

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 oceanwaters

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.

Modern marine calcified cyanobacteria 3


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 cyano-

bacteria 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 cyanobacte-

ria, Dichothrix, form the calcified filaments that define the

unlaminated tuffs on the Highborne Cay thrombolitic struc-

tures. 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

presence of basal heterocytes, obligatory sheaths, narrowing

apical ends, and a lack of akinetes. All observedDichothrix fila-ments have some degree of calcification, but the initial calcifi-

cation was rarely observed to complete coat the filaments.

Other cyanobacteria can be present within the tuffs, including

cyanobacteria in genus Oscillatoria. The Oscillatoria, in con-

trast 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 autofluores-

cence (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

A

B

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) Micro-

bialite 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.

A

B

Fig. 3 Photos of the calcified cyanobacterial filaments. (A) Photo of a tuft of

vertically oriented calcifiedDichothrix filaments from the surface of a thrombo-

litic microbialites. Scale bar is 1 cm. (B) Photo showing the carbonate coating on

Dichothrix filaments. Scale 1 mm.



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 themicrobialite grade gradually downward from the

surface into poorly defined, degraded calcified cells and associ-

ated fine-grained, micrite precipitates (Fig. 5). The mucilagi-

nous sheaths in degraded cyanobacterial cells are typically

absent or non-continous (Figs 5B and 6B). Carbonate precip-

itates 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 experi-

enced 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 precip-

itate 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 dia-

genetic progression – fromwell-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 themicrobial 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 micriti-

zation is common. In some cases, the tuffs of calcified

filaments are growing on a distinct micritization front.

A B

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.

A

B

C

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 microfos-

sils would not be preserved in the geological record. Scale bars 100 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 stromat-

olites 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 unlaminatedmicro-

bialites 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,

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 micro-

bialites, and the precipitates from the adjacent stromatolites

(Andres et al., 2006). Three samples of calcified filaments

display d18O values £+1& (Fig. 8).

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 cyanobacteri-

al community (Myshrall et al., 2008). The presence of some

degree of sheath calcification in all of the observedDichothrixfilaments 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 calcifica-tion (Fig. 9).

A B

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.

–1

0

1

2

3 4 5 6(‰ VPDB)!13C

!18 O

(‰ V

PD

B)

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).

A

B

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 degrada-

tion. 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.



The presence in vivo calcification within the Dichothrixsheath is consistent with photosynthesis-induced carbonate

precipitation: cyanobacterial sheaths experience a significant

increase in pH during photosynthesis due to carbon dioxide

uptake (Visscher & vanGemerden, 1991; Arp et al., 2001).Carbon dioxide degassing is not inducing carbonate precip-

itation 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. Dichothrixfilaments 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 diox-

ide 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 precipi-

tates 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 precipi-

tation in an environment with bicarbonate derived from isoto-

pically light organic matter remineralization (Andres et al.,2006).

Significantly more positive d13C values in the calcified fila-

ments of the thrombolitic microbialites – compared to

those in the adjacent stromatolite precipitates or the sur-

rounding 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

Fig. 9 Schematic showing the stages of formation

and degradation of calcified cyanobacterial fila-

ments in Highborne Cay microbialites. See text for

further details.



carbonate d13C values cannot be used to quantitatively resolve

DIC reservoir shifts. Highborne Cay sediments have signifi-

cantly lower d13C values than the calcified filament precipi-

tates, 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 photosyn-

thetic 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 heterotro-

phic activitywere found in sectionsofBahamianmicrobialmats

with living, highly productive cyanobacteria than in sections

with decaying cyanobacteria (including heterotrophicmetabo-

lisms likely to induce carbonate precipitation like sulfate reduc-

tion) (Visscher et al., 2000; Braissant et al., 2009). Therefore,it is likely that the initial carbonate precipitates in theDichothrixsheath 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 theDichothrix sheath precipitates. Further, moremicrobi-

ologically oriented research will be required to elucidate the

relative importance of heterotrophic and photosynthetic

activity in causing the initialDichothrix filament calcification.

The absence of filament calcification in cyanobacteria other

than Dichothrix at Highborne Cay may be linked with differ-

ences in EPS composition, since EPS has been shown to have

a strong influence on the style and extent of microbial calcifi-

cation (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 byDichotrix 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 hetero-

trophic bacteria, effectively reducing the cation-binding

potential. Furthermore, if the dense clusters of cyanobacteria

in the thrombolites locally have very high rates of photosyn-

thesis, 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 condi-

tions for precipitation, it also causes the EPS to form gels

(Sutherland, 2001) potentially eliminating inhibition of car-

bonate precipitation. The different calcification mechanisms

at Highborne Cay clearly indicate that benthic microbial com-

munities can have a strong control on the type of microbial

carbonate precipitation.

The Highborne Cay thrombolitic microbialites demon-

strate 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 arago-

nite fabric is a contrast to that present in calcified filaments

that have undergone little structural degradation, where

aragonite crystals are acicular and distinct. Localized dissolu-

tion–reprecipitation is common in a wide range of modern

shallow marine carbonates (Reid & MacIntyre, 1998) includ-

ing subtidal Bahamian microbialites (Planavsky & Ginsburg,

2009). Carbonate under-saturation is likely induced by a com-

bination 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 calcifiedcyanobacteria

Our study offers insights into the factors controlling the tem-

poral distribution of calcified cyanobacteria microfossils

(Fig. 10). The rarity of these microfossils since the early Cre-

taceous (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 petrol-

ogy) 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 cyanobac-

terial filaments in several modern marine localities reveals that



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 (Ridg-

well, 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 dissolu-

tion 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 microfos-

sils 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 sig-

nificant factors controlling the number of occurrences ⁄abundance of calcified cyanobacterial microfossils in the Phan-

erozoic.

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 pre-

dominately 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 preser-

vation 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 Creta-

ceous. 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 transi-

tions 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).

0 100 200 500

4

6

8

10

20

40

60

0

20

40

60

80

Sur

face

"ca

lcite

[Ca+2

](m

mol

Kg–1

)

Rep

orte

d oc

cure

nces

of c

yano

bact

eria

calc

imic

rofo

ssils

/10

Ma

B

A

C

Age (Ma)300 400

COSDCTr PmJKCeno

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 Phanero-

zoic 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 produc-

tion occurring exclusively on shelf environments (upper black line) (from

Ridgwell, 2005). The formation and early diagenetic destruction of calcified fila-

ments 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 forma-

tion due to low calcium or carbonate ion concentrations.



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 withinthe cyanobacterial sheath. The calcified filaments have signifi-

cantly more positive carbonate d13C isotope values than

precipitates from adjacent stromatolites or than the surround-

ing sediment. These isotopic values suggest photosynthetic

activity was the central process driving carbonate precipitation

in the sheaths ofDichothrix 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 theHighborne 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 theOcean andResearch and Educa-

tion 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

AmericaGraduate StudentResearchFund. PTVacknowledges

support from NASA JRI through the Ames Research Center.

NP is greatly indebted to Robert Ginsburg for discussion and

guidance.Themanuscriptwas improveddue to insightful com-

ments from three anonymous reviewers and Lee Kump and

benefited from discussions with Noel James, Guy Narbonne,

andMarkPalmer.This isRIBSContribution#58.

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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.

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directed to the corresponding author for the article.

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