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 ANDP.T.VISSCHER3 1Rosenstiel School of Marine and Atmospheric Sciences, Miami, FL, USA 2Department of Earth Sciences, University of California, Riverside, Riverside, CA, USA 3Department 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 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 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]

marine cyanobacterial microfossils (Knoll et al., 1993; Dupraz INTRODUCTION et al., in press). Calcified cyanobacteria are found in several Calcified cyanobacteria microfossils are a common compo- marine environments (Winland & Matthews, 1974; Hardie, nent of marine carbonate reefs and sediments deposited from 1977; Riding, 1977; MacIntyre et al., 1996), but there has 550 to 100 Ma (Riding, 2000; Arp et al., 2001). Calcified- not been an extensive study of the calcification mechanisms in microfossils morphologies are diverse, and many have been any of these occurrences. The lack of a suitable, well-studied assigned formal taxonomic names (Riding, 2000). Filamen- modern analog for ancient marine calcified cyanobacteria has tous taxa, such Girvanella are likely the most common calci- fostered long-standing debate on the factors controlling the fied cyanobacteria, and have a morphology that can be directly formation, temporal distribution, and abundance of these related to modern cyanobacteria. These once common fossils microfossils (Knoll et al., 1993). are absent from the marine rock record since the Late Creta- The formation of calcified cyanobacterial microfossils is ulti- ceous (Sumner & Grotzinger, 1996; Arp et al., 2001; Riding mately caused by a local increase in calcium carbonate satura- & Liang, 2005). tion state driven by microbial metabolic activity. It has been Modern calcified cyanobacteria that are morphologically heavily debated if this shift in carbonate saturation state is comparable to ancient marine counterparts are commonly induced by cyanobacterial photosynthesis or heterotrophic found in freshwater settings and have been extensively studied microbial metabolisms (Visscher et al., 1998; Riding, 2000; (e.g. Merz, 1992). However, since freshwater systems have Arp et al., 2001; Dupraz & Visscher, 2005; Dupraz et al.,in carbonate and other major ion compositions that are dramati- press). Uptake of carbon dioxide during cyanobacterial cally different from those of marine settings, these modern photosynthesis increases the pH surrounding the cyanobacte- calcified cyanobacteria are not direct analogs for ancient rial cell, which favors carbonate precipitation. Bicarbonate is

566 2009 Blackwell Publishing Ltd Modern marine calcified cyanobacteria 567 the product of microbial sulfate and nitrate reduction, and its with sediments in the geological record and to understand the production also promotes calcium carbonate precipitation evolution of microbial carbonate production. (see Morse & MacKenzie, 1990; Dupraz & Visscher, 2005; Visscher & Stolz, 2005; Dupraz et al., in press for extensive STUDY AND LOCATION AND ENVIRONMENT reviews of the effects of different microbial metabolisms on calcium carbonate saturation state). These modes of calcified The calcified-cyanobacteria filaments are located in an open cyanobacteria formation – photosynthetic and organic matter marine environment at Highborne Cay (7649¢W, 2443¢N) remineralization induced carbonate precipitation – have typi- Exuma, Bahamas. Tufts of the filaments are found on throm- cally been viewed as part of a binary system (Turner et al., bolitic microbialites. These microbialites are up to a meter tall 2000; Arp et al., 2001; Kah & Riding, 2007). It has become and are located the intertidal region of the back reef of an increasingly clear that extrapolymeric substances (EPS) pro- algal-ridge fringing reef complex that extends for 2.5 km duced by cyanobacteria and heterotrophic bacteria also play a along the eastern shore of the Pleistocene island Highborne key role in calcification (e.g. Decho, 2000; Braissant et al., Cay (Fig. 1). Sampled thrombolitic microbialites are located 2007, 2009). Freshly produced EPS can have an inhibitory at Highborne Cay Sites 6 and 8 of Andres & Reid (2006). effect on calcification through binding of cations (e.g., Ca2+, Several of the thromboltic microbialites were found growing Mg2+; Dupraz & Visscher, 2005). When the cation-binding on top of 1084-year-old vermetid-gastropod shells, indicating capacity is saturated (Arp et al., 2003), or when EPS is recent growth (Planavsky and Reid, unpublished data). This degraded through microbial and ⁄ or physicochemical pro- age is based on radiometric (14C) dating performed on cesses, large amounts of Ca2+ ions are released, promoting cal- cleaned shell fragments using Accelerator Mass Spectrometry cification (Dupraz & Visscher, 2005). at Beta Analytical, Miami, Florida. The factors controlling the temporal distribution of calci- The Highborne Cay fringing reef complex contains fied cyanobacteria are also debated. Calcified cyanobacteria well-laminated stromatolites, in addition to the thrombolitic first appear in rock record in the middle Precambrian (Kah microbialites (Reid et al., 1999, 2000). The stromatolites are & Riding, 2007), but show a major increase in abundance also best developed in the back-reef setting. The reef is a in the early Cambrian (Arp et al., 2001). This Cambrian highly dynamic system, and all of the microbialites are periodi- event may have been caused by cyanobacterial evolution or cally covered by carbonate sand (Andres & Reid, 2006). major changes in the marine carbonic acid system (Walter & Continuous monitoring of the Highborne reef complex Heys, 1985; Knoll et al., 1993; Turner et al., 2000; Arp for over 2 years (2005–2006) indicates that there are peri- et al., 2001; Riding & Liang, 2005). Calcified cyanobacteria ods when eukaryotes – rather than cayanobacteria – are the are abundant through the most of the Paleozoic, but are dominant photosynthetic organisms on the surfaces of rare or absent for periods in the Mesozoic. Notably, calcified thromboltic microbialites. The eukaryotes include green cyanobacteria are rare in the Permian and Early Jurassic, algae, red algae, and a pink layer rich in EPS and spherical despite the presence of microbial carbonates during this spores, which have not received proper taxonomic treatment time period. Arp et al. (2001) proposed that the rarity of (see Littler et al., 2005, for discussion of Highborne Cay mid-Mesozoic calcified cyanobacteria is linked with low algae). Micritic aragonite precipitates in the pink layer form- marine calcium concentrations. Calcified cyanobacteria are ing crude laminations at the top of nearshore buildups (Reid rare in the Cretaceous and disappear from the marine rock et al., 1999). Except for these micritic laminations, the record in the Late Cretaceous. Their absence over the past thrombolitic microbialites have clotted and mottled fabrics 65 Ma is thought to be due to low marine calcium or (Fig. 2) (Reid et al., 1999). carbonate ion concentrations, which would have lowered the calcium carbonate saturation state and inhibited micro- MATERIALS AND METHODS fossil formation (Sumner & Grotzinger, 1996; Riding, 2000; Arp et al., 2001). Cyanobacterial mats were examined within an hour of collec- Here we describe calcified cyanobacterial filaments from a tion using light and fluorescence microscopy. The fluores- modern marine setting at Highborne Cay in the Bahamas. We cence microscope (using a 490-nm excitation filter) was used document the growth and early diagenetic history of the to visualize carbonate precipitates and examine the degree of calcified cyanobacteria at Highborne – presenting information cyanobacterial autoflorescence. Cyanobacterial fluorescence, from field observations, petrographic examinations, and stable as viewed with the 490-nm excitation filter, is caused by isotope work. Our documentation of a modern marine calcify- accessory photosynthetic pigments – predominately phyco- ing cyanobacterium allows us to test models that explain the biliproteins – and can thus be used to estimate photosynthetic formation, temporal distribution, and abundance of ancient ability. calcified cyanobacteria. Our study strengthens the view that Clusters of cyanobacterial cells were fixed in 4.5% gultarald- understanding the geochemical dynamics of modern hyde in sodium cacodylate buffered solution within an microbial ecosystems is essential to link microbial processes hour of collection for electron microscopy work. We did a

2009 Blackwell Publishing Ltd 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 calcified filaments were isolated from surrounding sediment at initial fixation. Material used for electron microcopy was 50· magnification using a dissecting microscope. The purity coated in palladium and viewed using a FEI ⁄ Philips XL30 of a subset of the calcified filament samples was checked using environmental scanning electron microscope (E-SEM) with scanning electron microscopy (SEM). All samples examined an Oxford L300Qi-Link ISIS EDS at University of Miami, using SEM contained minor amounts of sediment impurities. Department of Geology. The isotopic values, therefore, are a qualitative, rather than Our observations on the early diagenetic history of calcified truly quantitative, estimate of the calcified filament isotopic cyanobacteria are from 42 standard petrographic thin sec- values. tions. All material was embedded under vacuum with epoxy Carbonates were isotopically analyzed with a Kiel III prior to sectioning. Nineteen of these thin sections come from automated carbonate device interfaced to a Thermo Finnigan two complete thrombolitic microbialites excavated from Delta-plus stable isotope ratio mass spectrometer at the Stable Highborne Cay (Site 6 of Andres & Reid, 2006). The remain- Isotope Laboratory at the Rosenstiel School of Marine and ing thin sections are from the upper, surficial sections of Atmospheric Science, Miami Fl. Results were corrected for Highborne Cay thrombolitic microbialites. standard drift and isobaric interferences and are expressed We extracted calcified, autofluorescent cyanobacteria cells relative to Vienna Peedee belemnite. Instrument precision for carbonate carbon and oxygen isotopic analysis. The was better than 0.15& for d18Oandd13C(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) 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.

The carbonate mineralogy of filaments was determined using X-ray diffraction with a PAN alytical X’Pert X-ray Fig. 3 Photos of the calcified cyanobacterial filaments. (A) Photo of a tuft of diffractometer operated at the Stable Isotope Laboratory 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 the Rosenstiel School of Marine and Atmospheric Sciences. Dichothrix filaments. Scale 1 mm. Similar to the isotopic work, calcified, autofluorescent cyanobacteria cells were isolated from surrounding sediment using a dissecting microscope. Additionally, using electron dispersive presence of basal heterocytes, obligatory sheaths, narrowing spectroscopy (EDS) we were able to determine carbonate apical ends, and a lack of akinetes. All observed Dichothrix fila- mineralogy at the micron scale (see Planavsky & Ginsburg, ments have some degree of calcification, but the initial calcifi- 2009, for information about determining mineralogy with cation was rarely observed to complete coat the filaments. EDS). Other cyanobacteria can be present within the tuffs, including cyanobacteria in genus Oscillatoria.TheOscillatoria,incon- trast to the Dichothrix filaments, do not show well-defined RESULTS mucilaginous sheaths. Although, the tuffs are dominated by vertically oriented cyanobacteria (Fig. 3A), occasional red Description of calcified filaments algae may be interspersed, especially on the tops upper Calcified cyanobacteria filaments, along with trapped and surfaces of the more seaward microbialites. No carbonate bound sand grains, form unlaminated tuffs or buttons that precipitates were observed on the red algae or the adjacent cover the tops and sides of the thrombolitic microbialites. The sediment. tuffs are typically between 1 and 5 cm across and many are Initial calcification occurs around Dichothrix filaments that exposed at low tide (Fig. 3A). A single variety of cyanobacte- lack obvious signs of filament or sheath degradation (Figs 4A ria, Dichothrix, form the calcified filaments that define the and 5A). Surficial calcifying filaments are strongly autofluores- unlaminated tuffs on the Highborne Cay thrombolitic struc- cence (viewed with 490-nm excitation filter). The degree of tures. We identified the filaments as Dichothrix based on the autofluorescence in the Dichothrix cell decreases markedly presence of common lateral false branching, with the branch over a centimeter scale with depth in the filament tufts first running parallel to the original trichome, as well as the (Fig. 4B). The initial carbonate precipitation occurs in the

2009 Blackwell Publishing Ltd 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 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 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 Fig. 5 (A–C) Light micrographs illustrating the early diagenetic transition from fibrous aragonite cement is locally abundant. The lower distinct calcified cyanobacterial filaments to patchy fine-grained carbonate cements. The light micrographs in A–C are taken from a single microbialite over sections of the microbialites are also heavily bored and locally a 7-cm vertical distance. Calcified filaments are also absent from more basal contain abundant encrusting foraminifera. Extensive micriti- sections of the microbialite indicating that the calcified cyanobacterial microfos- zation is common. In some cases, the tuffs of calcified sils would not be preserved in the geological record. Scale bars 100 lm. filaments are growing on a distinct micritization front.

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 DISCUSSION 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 Formation of calcified cyanobacteria l 10 m. 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 Stable isotope results uppermost section of the Dichothrix tufts, where there are Carbonate from the calcified filaments has d13C isotope values high rates of photosynthesis indicating an active cyanobacteri- ranging from +4.50& to +5.82& (Fig. 8). Detrital carbonate al community (Myshrall et al., 2008). The presence of some grains and fine-grained precipitates from the adjacent stromat- degree of sheath calcification in all of the observed Dichothrix olites at Highborne Cay have a range of d13C values from filaments provides strong support for calcification occurring +4.61& to +4.83& and +3.1& to +4.58& respectively during the cyanobacterial life cycle. Strong autofluorescence (Andres et al., 2006). Bulk samples of the unlaminated micro- in surficial calcified cells likely indicates photosynthetic ability. bialites have carbonate d13C values that range from +4.3% to The lack of obvious signs of heterotrophic degradation in the +4.79& (Fig. 8). The d13C values of the calcified filaments initial calcified cells also provides support for in vivo calcifica- are significantly higher than the Highborne Cay sediments, tion (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 ﬁla- ments in Highborne Cay microbialites. See text for further details.

The presence in vivo calcification within the Dichothrix of calcification is distinctly different in each microbialite type. sheath is consistent with photosynthesis-induced carbonate The micritic laminations in the Highborne Cay stromatolites precipitation: cyanobacterial sheaths experience a significant precipitate in a zone of localized, intense sulfate reduction increase in pH during photosynthesis due to carbon dioxide (Visscher et al., 2000). This correlation was shown through uptake (Visscher & van Gemerden, 1991; Arp et al., 2001). silver-foil experiments in the microbial ecosystems forming Carbon dioxide degassing is not inducing carbonate precip- the stromatolites, which track microbial sulfide production itation within the Dichothrix tufts. The lack of carbonate from sulfate (Visscher et al., 2000). The stromatolite precipi- precipitation on the red algae interspersed with the calcifying tates contain carbon isotope values that are lower than would filaments or the adjacent sediment is inconsistent with carbon be predicted if precipitation occurred from the ambient dioxide degassing driving carbonate precipitation. Dichothrix dissolved inorganic carbon (DIC) reservoir (Andres et al., filaments are calcifying on the sides of microbialites that are 2006). The light d13C isotope values are likely due to precipi- unaffected by exposure. Further, oxygen isotopes from the tation in an environment with bicarbonate derived from isoto- carbonate precipitates from Dichothrix sheaths, with limited pically light organic matter remineralization (Andres et al., exception, do not show an evaporative signal (carbonate with 2006). high d18O values). An evaporative signal would likely be Significantly more positive d13C values in the calcified fila- present if carbon dioxide degassing linked with elevated ments of the thrombolitic microbialites – compared to temperatures had driven calcification. However, carbon diox- those in the adjacent stromatolite precipitates or the sur- ide degassing can also be caused by increased agitation, which rounding sediment – suggests carbonate precipitation in the would not result in an evaporative signature in carbonate sheath of these filaments was in part photosynthetically oxygen isotope values. induced. During cyanobacterial photosynthesis, preferential The carbonate d13C isotope values from Highborne Cay uptake of 12C-enriched carbon dioxide or bicarbonate creates microbialites provide additional insights into the mechanisms a 13C-enriched microenvironment with an elevated pH in the driving calcium carbonate precipitation. Significantly more mucilaginous sheath (for review see Riding, 2000, 2006). positive d13C isotope values in the calcified filaments than in Since the calcified filaments analyzed isotopically contained the adjacent stromatolite precipitates indicate that the mode minor amounts of contaminating carbonate sediment, the

2009 Blackwell Publishing Ltd Modern marine calcified cyanobacteria 573 carbonate d13C values cannot be used to quantitatively resolve The Highborne Cay thrombolitic microbialites demon- DIC reservoir shifts. Highborne Cay sediments have signifi- strate that penecontemporaneous diagenesis can have a strong cantly lower d13C values than the calcified filament precipi- influence on microbial carbonate fabrics. Abundant carbonate tates, indicating the true values of these precipitates are precipitation occurs after the initial, in vivo calcification that slightly higher than reported. forms the calcified filaments. The loss of the distinct shape of Dichothrix filaments have a different calcification history the calcified cells suggests that there is localized carbonate than the Schizothrix filaments in adjacent stromatolites. Initial dissolution as well as precipitation of secondary carbonate calcification in Dichothrix is occurring in vivo and photosyn- cements during early diagenesis (Fig. 9). The fine-scale thetic activity appears to be one of the processes inducing microstructures in the calcified filaments provide additional calcification. There is no evidence for in vivo calcification of evidence for carbonate dissolution. The fused and indistinct Schizothrix filaments (Reid et al., 2000; Visscher et al., 2000; aragonite crystals present in the Dichotrix sheaths that have Andres et al., 2006). However, this does not support that undergone structural degradation are indicative of multiple initial Dichothrix calcification is a strictly photosynthetically stages of aragonite dissolution and reprecipitation (Macintyre induced process. In previous work, higher rates of heterotro- & Reid, 1995; Reid & MacIntyre, 1998). This altered arago- phic activity were found in sections of Bahamian microbial mats nite fabric is a contrast to that present in calcified filaments with living, highly productive cyanobacteria than in sections that have undergone little structural degradation, where with decaying cyanobacteria (including heterotrophic metabo- aragonite crystals are acicular and distinct. Localized dissolu- lisms likely to induce carbonate precipitation like sulfate reduction–reprecipitation is common in a wide range of modern tion) (Visscher et al., 2000; Braissant et al., 2009). Therefore, shallow marine carbonates (Reid & MacIntyre, 1998) includ- it is likely that the initial carbonate precipitates in the Dichothrix ing subtidal Bahamian microbialites (Planavsky & Ginsburg, sheath are linked with both heterotrophic and photosynthetic 2009). Carbonate under-saturation is likely induced by a com- activity. This interpretation is consistent with the presence of bination of sulfide production during initial stages of sulfate distinct but small differences in carbon isotope values between reduction, sulfide oxidation, and aerobic respiration (Morse the likely heterotrophically induced stromatolite precipitates & MacKenzie, 1990; Walter et al., 1993; Visscher et al., and the Dichothrix sheath precipitates. Further, more microbi- 1998; Dupraz & Visscher, 2005; Visscher & Stolz, 2005; Hu ologically oriented research will be required to elucidate the & Burdige, 2007). relative importance of heterotrophic and photosynthetic activity in causing the initial Dichothrix filament calcification. Temporal distribution and abundance of calcified The absence of filament calcification in cyanobacteria other cyanobacteria than Dichothrix at Highborne Cay may be linked with differences in EPS composition, since EPS has been shown to have Our study offers insights into the factors controlling the tem- a strong influence on the style and extent of microbial calcifi- poral distribution of calcified cyanobacteria microfossils cation (e.g. Braissant et al., 2007; Dupraz et al., in press). (Fig. 10). The rarity of these microfossils since the early Cre- The EPS of the sheathed cyanobacteria Schizothrix, the taceous (around 145 Ma) (Fig. 10A) has been linked with dominant cyanobacteria in the stromatolites at Highborne inhibited fossil formation due to low Ca concentrations (and Cay, initially has a strong inhibitory effect on carbonate hence a lower calcium carbonate saturation state) (Arp et al., precipitation (Kawaguchi & Decho, 2002). It is possible that 2001). Calcium concentration drawdown was linked with the the EPS produced by Dichotrix has less pronounced inhibitory radiation of planktonic calcareous algae such as coccoliths effect on calcification (e.g. through a reduced Ca-binding (Arp et al., 2001). This model of ocean chemistry is at odds capacity compared to other cyanobacterial EPS), allowing for with modeling work on Phanerozoic cation concentrations, sheath calcification. Alternatively, the local production of EPS which suggest that the Cretaceous contained the highest Ca2+ by Dichotrix could be in balance with degradation by hetero- concentrations in the Phanerozoic (Fig. 10B) (Hardie, 1996; trophic bacteria, effectively reducing the cation-binding Lowenstein et al., 2001). The model of Hardie (1996) does potential. Furthermore, if the dense clusters of cyanobacteria not take into account the effects planktonic calcareous algae in the thrombolites locally have very high rates of photosyn- radiation (Arp et al., 2001), but (based on carbonate petrol- thesis, this will result in a pH increase, as is typically observed ogy) the early Cretaceous appears to be a ‘calcite sea’ time in microbial mats (Revsbech & Jørgensen, 1986; Visscher period (e.g. Sandberg, 1983), which is consistent with high et al., 1991). The elevated pH not only favors chemical condi- Ca2+ concentrations (Lowenstein et al., 2001). Coccolith tions for precipitation, it also causes the EPS to form gels radiation is also inferred to have lowered the global marine (Sutherland, 2001) potentially eliminating inhibition of car- carbonate saturation state by decreasing the carbonate ion bonate precipitation. The different calcification mechanisms concentrations, which – again – may have decreased the ability at Highborne Cay clearly indicate that benthic microbial com- of cyanobacteria to from calcified microfossils (Riding, 2000). munities can have a strong control on the type of microbial However, the widespread occurrence of calcifying cyanobac- carbonate precipitation. terial filaments in several modern marine localities reveals that

2009 Blackwell Publishing Ltd 574 N. PLANAVSKY et al.

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 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 Fig. 10 (A) Reported occurrences of calcified cyanobacteria microfossils per occurrences of calcified cyanobacteria than in the Permian. It 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 is likely, therefore, that inhibited formation of calcified squares; Horita et al., 2002) estimates of Ca concentration throughout the cyanobacteria and possibly rock abundance biases are also sig- Phanerozoic. (C) Model of surface calcite saturation state through the Phanero- nificant factors controlling the number of occurrences ⁄ zoic in an ocean with deep-sea carbonate burial caused by a rain of calcified abundance of calcified cyanobacterial microfossils in the Phan- planktonic organisms (lower black line) and in an ocean with carbonate produc- erozoic. tion occurring exclusively on shelf environments (upper black line) (from Ridgwell, 2005). The formation and early diagenetic destruction of calcified fila- The abundance of calcified filaments in the late Jurassic ments in the modern oceans suggests that the low abundance of calcified (Fig. 10A) indicates an interval of high preservation and cyanobacterial microfossils over last 150 Ma and from 250 to 300 Ma may be calcifying potential. This is at odds with models that suggest the results of low preservation potential as well as inhibited microfossil forma- that the restructuring of the carbon cycle to a system with pre- tion due to low calcium or carbonate ion concentrations. dominately deep-sea carbonate deposition occurred by this time. As discussed above, the shift to a deep-sea-dominated precursors to these microfossils can form in modern oceans. carbonate cycle would have likely greatly decreased the preser- Besides Highborne Cay, calcified filaments are common in the vation and calcifying potential of calcified cyanobacteria. reef tract off Stocking Island (eastern Bahamas) (MacIntyre Therefore, although there was a large increase in diversity and et al., 1996) in carbonate sands on the eastern Bahama Bank abundance of calcifying pelagic organisms in the Jurassic (Winland & Matthews, 1974) in peritidal environments off (Martin, 1995), it appears they did not become abundant Andros Island (western Bahamas) (Hardie, 1977), and in enough to revolutionize the carbon cycle until the Creta- pools on Aldabra Atoll (Seychelles) (Riding, 1977). Their ceous. This is in accordance with sedimentological evidence presence is significant since modern oceans are inferred to that suggests deep-sea carbonate burial increased throughout contain some of the lowest marine Ca2+ concentrations the Mesozoic and reached it zenith during the Cretaceous (Hardie, 1996; Lowenstein et al., 2001) and have close to the (Siesser, 1993). Thus, the record of calcified cyanobacteria lowest levels of carbonate supersaturation (Ridgwell, 2005; provides insights into the timing of one of the major transi- Ridgwell & Zeebe, 2005) in the Phanerozoic (Fig. 10B). The tions in Earth’s history and biosphere that is difficult to gauge limited number of occurrences of calcified filaments in the through traditional proxies, such as the diversity of calcifying modern oceans, however, demonstrates that cyanobacteria pelagic organisms (Martin, 1995) or the percent of ophilite filament calcification is not a ubiquitous process. complexes containing carbonate (Boss & Wilkinson, 1991).

2009 Blackwell Publishing Ltd Modern marine calciﬁed cyanobacteria 575

These traditional proxies for pelagic carbonate production are Arp G, Reimer A, Reitner J (2003) Microbialite formation in seawater only weakly linked to amount of carbonate deposition. of increased alkalinity, Satonda Crater Lake, Indonesia. Journal of Sedimentary Research 73, 105–117. Boss SK, Wilkinson BH (1991) Planktogenic eustatic control on cratonic CONCLUSIONS oceanic carbonate accumulation. Journal of Geology 99, 497–513. Braissant O, Decho AW, Dupraz C, Glunk C, Przekop KM, Visscher We documented the formation and early diagenetic history PT (2007) Exopolymeric substances of sulfate-reducing bacteria: of calcified cyanobacteria from a modern open marine setting interactions with calcium at alkaline pH and implications for forma- at Highborne Cay, Bahamas. A single variety of cyanobacteria tion of carbonate minerals. Geobiology 5, 401–411. Braissant O, Decho AW, Przekop KM, Gallagher KL, Glunk C, at Highborne Cay, identified as Dichothrix sp., produce the Dupraz C, Visscher PT (2009) Characteristics and turnover of exo- calcified filaments. Calcification initially occurs in vivo within polymeric substances in a hypersaline microbial mat. FEMS Microbi- the cyanobacterial sheath. The calcified filaments have signifi- ology Ecology 67, 293–307. cantly more positive carbonate d13C isotope values than Decho AW (2000) Exopolymer-mediated microdomains as a precipitates from adjacent stromatolites or than the surround- structuring agent for microbial activities. In Microbial Sediments (eds Riding R, Awramik SM). Springer-Verlag, Berlin, pp. ing sediment. These isotopic values suggest photosynthetic 9–15. activity was the central process driving carbonate precipitation Dupraz CD, Visscher PT (2005) Microbial lithification in marine in the sheaths of Dichothrix cells. Variation in the calcification stromatolites and hypersaline mats. TRENDS in Microbiology 13, styles of Highborne Cay benthic ecosystems [e.g. formation 429–438. of well-laminated stromatolites versus (non-laminated) Dupraz CD, Reid PR, Braissant O, Decho AW, Norman SR, Visscher PT (in press) Processes of carbonate precipitation in modern micro- thrombolitic microbialites] clearly indicates that there can be a bial mats. Earth-Science Reviews. strong ecosystem control on microbial calcification. Hardie LA, ed. (1977) Sedimentation on the modern carbonate tidal During early diagenesis, the calcified filaments are degraded flats of northwest Andros Island, Bahamas. Johns Hopkins and there is abundant carbonate precipitation. The lack of University Studies in Geology 22, 202. preservation of the Highborne Cay calcified filaments suggests Hardie LA (1996) Secular variation in seawater chemistry: an explana- tion for the coupled secular variation in the mineralogies of marine that the absence of calcified cyanobacteria from periods in the limestones and potash evaporites over the past 600 my. Geology 24, Phanerozoic does not necessarily imply inhibited formation. 279–283. Poor preservation potential is likely a factor responsible for the Horita J, Heide Zimmermann H, Holland HD (2007) Chemical lack of marine calcified cyanobacterial fossils over the past evolution of seawater during the Phanerozoic: implications from 65 Myr as well as inhibited formation. the record of marine evaporates. Geochimica et Cosmochimica Acta 66, 3733–3756. Hu XP, Burdige DJ (2007) Enriched stable carbon isotopes in the ACKNOWLEDGEMENTS pore waters of carbonate sediments dominated by seagrasses: evidence for coupled carbonate dissolution and reprecipitation. NP received support from the Ocean and Research and Educa- Geochimica et Cosmochimica Acta 71, 129–144. tion Fund. RPR acknowledges support from NSF grant EAR Kah LC, Riding R (2007) Mesoproterozoic carbon dioxide levels inferred from calcified cyanobacteria. Geology 35, 799–802. 0221796 and TWL from the NASA Exobiology program. Kawaguchi T, Decho AW (2002) Isolation and biochemical character- KLM received funding from the Paleontological Society ization of extracellular polymeric secretions (EPS) from modern Grant-In-Aid program and from the Geological Society of soft marine stromatolites (Bahamas) and its inhibitory effect on America Graduate Student Research Fund. PTV acknowledges CaCO3 precipitation. Preparative Biochemistry & Biotechnology support from NASA JRI through the Ames Research Center. 32, 51–63. Knoll AH, Fairchild IJ, Swett K (1993) Calcified microbes in Neopro- NP is greatly indebted to Robert Ginsburg for discussion and terozoic carbonates – implications for our understanding of the guidance. The manuscript was improved due to insightful com- Proterozoic Cambrian transition. Palaios 8, 512–525. ments from three anonymous reviewers and Lee Kump and Littler DS, Littler MM, Macintyre IG, Bowlin E, Andres MS, Reid RP benefited from discussions with Noel James, Guy Narbonne, (2005) Guide to the dominant macroalgae of the stromatolite and Mark Palmer. This is RIBS Contribution #58. fringing reef complex, Highborne Cay, Bahamas. Atoll Research Bulletin 532, 67–92. Lowenstein TK, Timofeeff MN, Brennan ST, Hardie LA, Demicco REFERENCES RV (2001) Oscillations in Phanerozoic seawater chemistry: evidence from fluid inclusions. Science 294, 1086–1088. Andres MS, Reid RP (2006) Growth morphologies of modern marine Macintyre IG, Reid RP (1995) Crystal alteration in a living calcareous stromatolites: a case study from Highborne Cay, Bahamas. alga (Halimeda) – implications for studies in skeletal diagenesis. Sedimentary Geology 185, 319–328. Journal of Sedimentary Research 65, 143–153. Andres MS, Sumner DY, Reid RP, Swart PK (2006) Isotopic finger- MacIntyre IG, Reid PR, Stenck RS (1996) Growth history of stromat- prints of microbial respiration in aragonite from Bahamian stromatolites in a Holocene fringing reef, Stocking Island, Bahamas. olites. Geology 34, 973–976. Journal of Sedimentary Research 66, 231–242. Arp G, Reimer A, Reitner J (2001) Photosynthesis-induced biofilm Martin RE (1995) Cyclic and secular variation in microfossil biomin- calcification and calcium concentrations in Phanerozoic oceans. eralization – clues to the biogeochemical evolution of Phanerozoic Science 292, 1701–1704. oceans. Global and Planetary Change 11, 1–23.

2009 Blackwell Publishing Ltd 576 N. PLANAVSKY et al.

Merz MUE (1992) The biology of carbonate precipitation by Sutherland IW (2001) Biofilm exopolysaccharides: a strong and sticky cyanobacteria. Facies 26, 81–101. framework. Microbiology 147, 3–9. Morse J, MacKenzie F (1990) Geochemistry of Sedimentary Turner EC, James NP, Narbonne GM (2000) Taphonomic control Carbonates. Elsevier, Amsterdam. on microstructure in early neoproterozoic reefal stromatolites and Myshrall KL, Norman RS, Thompson JB, Visscher PT (2008) Micro- thrombolites. Palaios 15, 87–111. bial community composition in modern thrombolites: a compari- Visscher PT, Stolz JF (2005) Microbial mats as bioreactors: popula- son of open marine and freshwater systems using molecular tions, processes, and products. Palaeogeography, Palaeoclimatology, techniques. Geological Society of America Abstracts with Programs Palaeoecology 219, 87–100. 40, 412. Visscher PT, van Gemerden H (1991) Production and consumption Planavsky N, Ginsburg RN (2009) Thaponomy of modern marine of dimethyl-sulfoniopropionate in marine microbial mats. Applied Bahamian microbialites. Palaios 24, 5–24. and Environmental Microbiology 57, 3237–3242. Reid RP, MacIntyre IG (1998) Carbonate recrystallization in shallow Visscher PT, Quist P, van Gemerden H (1991) Methylated sulfur marine environments: a widespread diagenetic process forming compounds in microbial mats: in situ concentrations and metabo- micritized grains. Journal of Sedimentary Research 68, lism by a colorless sulfur bacterium. Applied and Environmental 928–946. Microbiology 57, 1758–1763. Reid RP, Macintyre IG, Steneck R (1999) A microbialite ⁄ algal ridge Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG, Thomp- fringing reef complex, Highborne Cay, Bahamas. Atoll Research son J Jr (1998) Formation of lithified micritic laminae in modern Bulletin 466, 1–18. marine stromatolites (Bahamas): the role of sulfur cycling. Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, American Mineralogist 83, 1482–1491. Macintyre IG, Paerl HW, Pinckney JL, Prufert-Bebout L, Steppe Visscher PT, Reid RP, Bebout BM (2000) Microscale observations of TF, DesMarais DJ (2000) The role of microbes in accretion, lami- sulfate reduction: correlation of microbial activity with lithified nation and early lithification of modern marine stromatolites. micritic laminae in modern marine stromatolites. Geology 28, Nature 406, 989–992. 919–922. Revsbech NP, Jørgensen BB (1986) Microelectrodes: their use in Walter MR, Heys GR (1985) Links between the rise of the metazoa microbial ecology. Advances in Microbial Ecology 9, 293–352. and the decline of stromatolites. Precambrian Research 29, Ridgwell A (2005) A mid Mesozoic revolution in the regulation of 149–174. ocean chemistry. Marine Geology 217, 339–357. Walter LM, Bischof SA, Patterson WP, Lyons TW (1993) Dissolution Ridgwell A, Zeebe RE (2005) The role of the global carbonate cycle and recrystallization in modern shelf carbonates – evidence from in the regulation and evolution of the Earth system. Earth and pore-water and solid-phase chemistry. Philosophical Transactions of Planetary Science Letters 234, 299–315. the Royal Society of London, Series A 344, 27–36. Riding R (1977) Calcified Plectonema (blue-green algae), a recent Winland HD, Matthews RK (1974) Origin and significance of grape- example of Girvanella from Aldabra Atoll. Palaeontology 20, 33–46. stone, Bahama Islands. Journal of Sedimentary Petrology 44, Riding R (2000) Microbial carbonates: the geological record of calci- 921–927. fied bacterial-algal mats and biofilms. Sedimentology 47, 179–214. Riding R (2006) Cyanobacterial calcification, carbon dioxide concen- trating mechanisms, and Proterozoic-Cambrian changes in atmo- SUPPORTING INFORMATION spheric composition. Geobiology 4, 299–316. Riding R, Liang LY (2005) Geobiology of microbial carbonates: Additional Supporting Information may be found in the metazoan and seawater saturation state influences on secular trends online version of this article: during the Phanerozoic. Palaeogeography Palaeoclimatology Palaeoecology 219, 101–115. Table S1 Stable isotope values and sample identification for data shown in Sandberg PA (1983) An oscillating trend in Phanerozoic non-skeletal main text Fig. 8. mineralogy. Nature 305, 19–22. Siesser W (1993) Calcareous nannoplankton. In Fossil Prokaryotes and Protists (ed. Lipps J). Blackwell Scientific, Oxford, pp. 169–201. Please note: Wiley-Blackwell is not responsible for the content Stanley SM, Hardie LA (1998) Secular oscillations in the carbonate or functionality of any supporting materials supplied by the mineralogy of reef-building and sediment-producing organisms authors. Any queries (other than missing material) should be driven by tectonically forced shifts in seawater chemistry. Palaeogeo- directed to the corresponding author for the article. graphy, 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.

2009 Blackwell Publishing Ltd