Spatial Distribution and Preservation of Carbon Isotope Biosignatures

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Article Cite This: ACS Earth Space Chem. XXXX, XXX, XXX−XXX

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Spatial Distribution and Preservation of Carbon Isotope Biosignatures in Freshwater Microbialite Carbonate Mark A. Belan,† Allyson L. Brady,† Sang-Tae Kim,† Darlene S. S. Lim,‡ and Greg F. Slater*,† †

School of Geography and Earth Sciences, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, Canada NASA Ames Research Center, Mail Stop 245-3, Moffett Field, California 94035, United States

‡

ACS Earth Space Chem. Downloaded from pubs.acs.org by IOWA STATE UNIV on 02/08/19. For personal use only.

S Supporting Information *

ABSTRACT: Understanding formation mechanisms of modern microbialites enables interpretation of biosignatures associated with fossilized stromatolites. Photosynthetic influences on carbonate precipitation are one proposed mechanism. Photosynthetic isotope biosignatures (13C) associated with freshwater microbialites in Pavilion Lake, British Columbia were widespread through the lake but less prevalent with increasing depth. Importantly, they were variably detectable on the exterior surface of individual microbialites. At depths ≤18 m, microbialite surface carbonates, associated with either nodular microbial communities or surface biofilms, had δ13Ccarb values up to +3.7‰ that were 13C-enriched above the predicted range of δ13Ccarb values for equilibrium precipitation from bulk ambient lake water dissolved inorganic carbon (DIC) (predicted mean δ13Ccarb = −0.2 ± 1.3‰). Vertical profiles of exterior, non-nodular biofilm present on microbialites collected from depths of 21 m and below showed instances of 13C-enrichment near the apex, consistent with hypothesized maximum light exposure. With increased distance from the apex toward the structure base, δ13Ccarb values typically decreased into the predicted range of equilibrium δ13C values. Surface biosignatures persisted internally for distances of 0.5 to 2 cm below the exterior of the structures, beyond which they fell within the predicted isotopic equilibrium range. This shift in δ13Ccarb values may be due to secondary carbonate precipitation masking of the 13C-enriched signature. The contribution of secondary carbonate precipitation was estimated to be 14−59% of total carbonate mass if derived from heterotroph-influenced or bulk lake DIC, respectively. Growth rate estimates suggested these accretion processes can mask photosynthetic signatures in 20−400 years. KEYWORDS: microbialite, biosignature, carbonate, carbon isotope, photosynthesis, preservation

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Lake13−15 and Kelly Lake.16 In contrast, biosignatures of heterotrophic activity, reflected as 12C-enrichment, have been identified in other modern microbialite systems such as Cuatro Ciénegas.17 Within the same geographic region, microbialites exhibiting biosignatures of both photosynthetic and heterotrophic influences on carbonate precipitation may be detected. For example, 13C-depletions within some Bahamian stromatolites reflect the role of heterotrophic processes,18,19 while nearby thrombolites show evidence of calcified cyanobacteria20 and exhibit 13C-enrichments associated with photosynthetic influences on carbonate precipitation.21 Understanding the variations in such biosignatures associated with microbialites provides the means to understand the biogeochemical processes contributing to their formation and the subsequent extension of this understanding to interpret microbialites that exist in the geologic record.22

INTRODUCTION Ancient laminated microbialites (e.g., stromatolites) ubiquitous throughout the geologic record are cited as some of the earliest records of life on Earth.1−4 Modern microbialites are organo-sedimentary structures5 with purported biogenic origins that are considered analogues of ancient microbialite and stromatolite forming systems. Microbialites are thought to form via several processes, including microbial trapping and binding of authigenic grains,6,7 creation of substrates for crystal nucleation,8,9 and/or induction of changes in local geochemical conditions resulting in carbonate precipitation.10,11 The latter mechanism is of primary interest as the induced changes in geochemical conditions have the potential to generate nonequilibrium carbon isotope effects that can be recorded within the precipitated carbonates as biosignatures.12 Detection of these biosignatures can provide insight into the mechanisms by which the microbialites were formed and the activities of associated biological systems. 13C-enrichment of carbonates due to photosynthetic preferential utilization of 12C has been observed within actively precipitating biofilm communities that dominate microbialite surfaces at Pavilion © XXXX American Chemical Society

Received: November 22, 2018 Revised: January 22, 2019 Accepted: January 23, 2019

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DOI: 10.1021/acsearthspacechem.8b00182 ACS Earth Space Chem. XXXX, XXX, XXX−XXX

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Figure 1. Map of Pavilion Lake, British Columbia, Canada (A). Freshwater microbialite samples representing various depths and sampling locations (B). Grid spacing is at centimeter intervals. The value located in the bottom right of each image refers to the total height measured (top to bottom) for each structure in centimeters. Note that 26 m is used to denote the deepest sample from these locations but that exact depths vary (e.g., the deepest sample from SBW was from a depth of 21 m). See text for further details.

above sea level. It is a freshwater, ultraoligotrophic lake with a mean pH of 8.3, is slightly supersaturated with respect to calcite (CaCO 3 ), develops a seasonal thermocline at approximately 10 m deep, and is comprised of three basins (North, Central, and South).28 Pavilion is host to an abundance of actively accreting microbialite structures that exhibit a wide range of morphologies varying with depth.23 This morphological variation has been hypothesized to result from changes in biological activity in different light regimes influencing precipitation.14,25,28 Microbialite and Water Chemistry Collection. Sampling of microbialites and water samples was performed at three distinct locations in Pavilion Lake: Three Poles (TP; 50.866N, 121.736W), South Basin East (SBE; 50.857N, 121.727W), and South Basin West (SBW; 50.853N, 121.725W) (Figure 1). SCUBA divers collected microbialite samples during the June 2014 field season at approximate depths of 10, 18, and 26 m. The microbialite samples from TP and SBW were collected at 26 and 27 m, respectively. Note that the deepest sample taken at SBE was from 21 m due to the lack of microbialites below that depth. Use of “ca. 26 m” throughout the text indicates the deepest samples collected from each of the three locations. Microbialites from ca. 10 m at all sites were selected randomly. However, based on previous findings,13 microbialites at ca. 18 m with visually distinct green and purple nodules were targeted at all locations. Due to limited microbialite development and lack of observed nodules in the North basin, samples were not collected for the current study. Due to the friable nature of the microbialites, particularly those from shallower depths, microbialite subsamples were removed in the field, and sections were embedded in Epotek 301 epoxy resin (Epoxy Technology Inc., Billerica, MA, United States) to preserve structural integrity of the samples and enable internal sampling. Resin was prepared according to manufacturer instructions. The remaining parent microbialites were frozen on-site and transported to McMaster University on dry ice for further analysis. Water samples for δ13C of DIC analysis were collected using 60 mL syringes by SCUBA divers as close to the corresponding

The lacustrine microbialites present in Pavilion Lake, BC, Canada are modern analogues of ancient stromatolite systems.23 Previous studies have identified high δ13Ccarb values observed for microbialites in water depths shallower than 20 m that were attributed to photosynthetic impacts on carbonate precipitation.13,14 However, these studies did not consistently detect 13C-enrichment within microbialite biofilms at depths below 20 m. This observation has been hypothesized to be a result of decreased relative rates of photosynthetic activity due to lower light levels and/or greater influence of heterotrophic metabolisms inputting isotopically light carbon (or 12C) to the local dissolved inorganic carbon (DIC) pool effectively masking any photosynthetic 13C-enrichment.13−15 These contrasting observations raise questions concerning the criteria for formation of 13C-enriched carbonate biosignatures and whether such signatures may vary spatially over the surface of individual Pavilion Lake microbialites. In addition, there has yet to be a determination of the extent to which these surface 13C-enrichments of carbonates persist within the interior of the Pavilion Lake microbialite structures. While morphological remnants of surface nodular microbial communities have been observed within the microbialites,24 evidence of secondary carbonate precipitation infilling the structures has also been observed.24,25 Such secondary precipitation raises the possibility that the original surface enrichment may be masked due to precipitation of carbonate from DIC that is either in isotope equilibrium with the bulk surface water DIC or is affected by inputs derived from heterotrophic activity beneath the microbialite surface.18,26,27 The goals of this study were to assess the spatial distribution of 13C-enriched biosignatures associated with the Pavilion Lake microbialites (including both within the lake itself and on the exterior of individual structures) as well as to better constrain the preservation potential of surface generated biosignatures within the interior of structures.

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EXPERIMENTAL SECTION Study Site. Pavilion Lake (5.7 × 0.8 km and 65 m deep) is located in south-central British Columbia, Canada, approximately 450 km northeast of Vancouver at an altitude of 823 m B

DOI: 10.1021/acsearthspacechem.8b00182 ACS Earth Space Chem. XXXX, XXX, XXX−XXX

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Figure 2. Bisected green nodule from South Basin West demonstrates banding of organic matter with precipitated carbonate bands clumped in between cyanobacterial filaments (A). Green and purple nodules were sectioned to constrain their growth (B and C) and cut into three sections representing the surface, interior, and basal components (D). Microbialite subsamples embedded in resin were used to create interior carbonate δ13C profiles from exterior surface to depths of up to ca. 6 cm (E).

resin. Sections were selected to enable sampling from the surface toward the center of the structure along apparent growth profiles as indicated by crystal orientation and overall structure morphology (Figure 2E). Resin embedded carbonate samples were cut at McMaster University with a tile saw and then sampled at 0.5 cm intervals along profiles starting from the microbialite exterior surface and extending approximately 3 to 6 cm deep into the structure. Intramicrobialite sampling profiles began directly at the microbialite surface, except for profiles beneath nodular surfaces, which began at the interface where the base of the nodule microstructure meets the general microbialite surface. Holes 2 × 2 mm were drilled with a micro electric hand drill, and approximately 0.1−0.3 mg of microbialite carbonate was collected. Stable Isotope Analysis. The carbon isotope composition of DIC (δ13CDIC) was determined by acidification and conversion to CO2 by an automated continuous flow isotope ratio mass spectrometer at the G.G. Hatch Laboratory in Ottawa, Canada.29 Carbon isotope analyses of carbonates (δ13Ccarb) were performed on a Gasbench and Finnigan DeltaPlus XP at 25 °C at McMaster University. Carbonates were not treated to remove organics prior to analysis because there is no consensus regarding proper pretreatment of biological carbonates and to remain consistent with previous studies on Pavilion Lake microbialites that did not pretreat carbonates.13 Testing of epoxy resin with Grenville Calcite Standard revealed δ13C contributions of +0.023 ± 0.008‰, considered negligible for the purposes of this study. All δ13C values are reported in standard delta (δ) notation in reference to Vienna PeeDee Belemnite (VPDB).

microbialite surface as possible at each location and depth within the lake. Water samples were transferred to screw cap glass bottles, fixed with mercuric chloride to prevent microbial activity, and sealed with no headspace prior to transfer to McMaster University for analysis. Microbialite Exterior Surface Sampling. Green and purple nodules were sampled from lyophilized microbialite surfaces using solvent rinsed forceps. Nodules were bisected and sectioned into three zones representing the surficial, internal, and basal sections of the nodule structure (Figures 2A−D). Based on the consistency of results from initial analysis of all three sections of nodules from TP, only surficial and basal sections from SBE and SBW were analyzed. Carbonates in association with surface biofilms (as described by Brady and colleagues14) from all sites and depths were also analyzed by collecting 1−3 mm-thick samples of biofilm from the microbialite surface using a solvent-rinsed scalpel. To investigate the distribution of biosignatures over the surface of individual microbialites, δ13Ccarb values were profiled from the apex to base on the denser microbialites collected from the deepest depths (i.e., 20+ m). Microbialites from these depths have not been habitually associated with 13C-enriched surface biofilm carbonate in previous studies. For the deepest samples from ca. 26 m depths, three vertical surface profiles of biofilm samples were collected along three different sides of individual microbialite structures at all sites. Triplicate samples were collected from each point. Surface profiles traversed along the microbialite surface from the apex toward the sediment water interface (SWI) and distances reported for exterior profile δ13C values are reported in cm measured relative to the apex. Microbialite Interior Carbonate Sampling. To assess the potential for preservation of surface δ13Ccarb biosignatures within the interior of the microbialite structure, internal depth profiles were generated. Carbonates were sampled from the exterior surface to up to 6 cm below the surface within the internal framework of the microbialites collected along the downslope transects within the lake. Pieces of microbialite 3−6 cm in length underlying surface nodules (both green and purple) and surface biofilm were sectioned and embedded in

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RESULTS Isotopic Composition of DIC. δ13CDIC values for all three sites and depths averaged −1.6 ± 0.3‰ (Supplementary Table 1). As calcite is enriched in 13C by +1.0 ± 0.2‰ above the bicarbonate from which it precipitates at isotopic equilibrium,30 the average predicted equilibrium δ13Ccarb value based on the mean measured lake δ13CDIC was −0.6 ± 0.3‰. This value falls within the range of predicted δ13Ccarb values for isotopic equilibrium precipitation originally proposed by Brady C

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ACS Earth and Space Chemistry et al. (−1.5 to +1.1 ‰; mean −0.2 ± 1.3‰).13 The isotopic equilibrium range proposed by Brady13 accounts for seasonal and temporal variation over a four-year period, and given the slow rate of carbonate precipitation in Pavilion Lake based on growth rate estimates (est. rate of 0.012 to 0.25 mm/year as in Brady et al;31 Brady unpublished data), the broader range proposed by Brady et al.13 was used as the basis of comparison in this study. Isotopic Composition of Surface Carbonates. Measured surface biofilm and nodule carbonate δ13Ccarb values are shown in Figure 3 (presented as mean ± SD). Here, nodule

Carbonates from surface profiles of microbialites collected from the deepest depths showed transitions from 13Cenrichment near the apex to δ13Ccarb values within the range predicted by isotopic equilibrium (Figure 4). At 21 m at SBE, δ13Ccarb values above the equilibrium range were identified for the entirety of Transect 2, while the other two transects transitioned into the predicted range of equilibrium values between 6 and 8 cm from the apex. At 26 m depth at TP, 13Cenrichment was strictly limited to the apex samples for Transect 1 before transitioning into the equilibrium range at ∼2 cm, while Transect 2 maintained 13C enrichment until ∼9 cm from the apex. δ13Ccarb values for Transect 3 were also above equilibrium at distances of up to 9 cm with the exception of a measurement at ∼2 cm that was within error of the equilibrium range. At 26 m depth at SBW, no 13Cenrichment outside of the range predicted by equilibrium were observed anywhere on the structure. Observed Trends in δ13C Values of Internal Microbialite Carbonate Profiles. δ13Ccarb values from intramicrobialite internal depth profiles are presented in Figure 5. The maximum δ13Ccarb values of +2.8 and +3.0‰ were recorded in samples collected from ca. 10 m water depth at TP and SBW respectively in green and purple nodules at the interface of these samples where the base of nodules attached to the bulk microbialite surface. Beneath this contact point, δ13Ccarb values decrease with increasing depth from the exterior surface until reaching the predicted equilibrium range at depths of ∼0.5 (SBW) and ∼1.5 cm (TP) below the exterior surface (Figure 5a). Internal carbonate profiles from 18 m microbialites demonstrated a similar trend, with maximum surface δ13Ccarb values of ∼+2.5‰ decreasing into the equilibrium range between 1.5 and 2 cm (Figure 5b). Microbialites sampled from water depths at and below 21 m generally do not show 13C-enrichment for the bulk of the profile. Surface carbonates near the apex of the representative SBE profile from 21 m have a δ13Ccarb value of ∼+1.5‰, slightly above the equilibrium range but rapidly decrease into the equilibrium range before reaching 0.5 cm depth below the exterior surface (Figure 5c). Within microbialites collected at deeper depths, measured δ13Ccarb values were typically within the predicted δ13Ccarb range of isotopic equilibrium precipitation, except for a single δ13Ccarb measurement from TP observed at ∼1.5 cm below the surface (Figure 5c).

Figure 3. Measured δ13C values of carbonate from microbialite surfaces at all sites and depths. Green and purple nodules are most common at 18 m. Surface carbonates from only one representative surface transect from ca. 26 and 27 m at each sampling site are included here.

δ13Ccarb values are the mean δ13Ccarb at a given depth as generated from the individual nodule profile means (surficial, internal, basal). All nodule δ13Ccarb values were higher than the range expected for carbonate in isotopic equilibrium with measured δ 13 C DIC values consistent with Brady and colleagues.13 The highest individual δ13Ccarb values measured were both +3.7‰ from the surficial nodule section of a green and purple nodule from SBE and SBW, respectively. At TP, the mean δ13Ccarb values of individual green nodules profiles ranged from +2.4 to +2.7‰ (mean δ13Ccarb values = +2.6 ± 0.5‰, n = 5). Purple nodule profile means ranged from +2.2 to +2.5‰ (mean +2.3 ± 0.5‰, n = 4). Nodule carbonates from SBE and SBW were similarly 13C-enriched: SBE nodule δ13Ccarb values from all depths ranged from +2.1 to +3.7‰ (green nodule mean +3.1 ± 0.7‰, purple mean +2.6 ± 0.4‰) and SBW δ13Ccarb values ranged from +1.7 to +3.7‰ (green nodule mean +2.8 ± 0.6‰, purple mean +2.8 ± 0.9‰). There was no evidence of systematic trends in carbon isotope composition between components of any of the nodules (surficial, internal, basal samples). Comparison of all nodule and surface biofilm carbonates identified an observable decrease in microbialite surface δ13Ccarb values that correlated with structure depth within the lake (Figure 3). To increase clarity, data from only one representative surface transect at each site at depths of ca. 26 are shown in Figure 3, but the trend is the same for all three surface transects, as seen in Figure 4. At 10 and 18 m depths, both nodular and surface carbonates were 13C-enriched above the predicted range of δ13Ccarb values for isotopic equilibrium precipitation (an exception was one surface biofilm from 18 m at TP), whereas carbonates from deeper samples trended toward the equilibrium range.

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DISCUSSION Photosynthetically 13C-enriched biosignatures were identified in most surface biofilm and nodule carbonates at all study sites at depths above 21 m, consistent with previous findings.14 The observation of 13C-enrichments in microbialite samples collected from the South Basin confirms that such biosignatures are not restricted to microbialites growing in the central basin of Pavilion Lake but are a widespread phenomenon. Furthermore, while previous studies had indicated that high δ13Ccarb values were present on some structures at depths of ca. 20 m and below,14 it was not clear whether such biosignatures were present over the entirety of the structure at these deeper depths. The current study addressed this outstanding question by demonstrating that surface δ13Ccarb values for samples from SBE at 21 m and TP at 26 m transition from being 13C-enriched relative to the isotopic equilibrium range at the apex of the structure to being within the equilibrium range closer to the sediment water interface (Figure 4). The extent of isotopic enrichment in D

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Figure 4. Measured δ13Ccarb values associated with surface carbonate transects demonstrating both photosynthetic enrichment near the apex of structures and δ13Ccarb values that were within the predicted equilibrium range. Three surface transects were measured on each structure. Triplicate measurements were made at each point. The shaded areas represent the proposed spatial distribution of photosynthetic biosignatures.

δ13Ccarb on the surface is hypothesized to be related to microbialite orientation with respect to the basin slope, with the outward (pelagic) facing surfaces showing the most extensive area of isotopic enrichment in samples from TP and SBE. In contrast, the sample from SBW at 26 m does not appear to show any trend with orientation. The observation of photosynthetic biosignatures at the apex of the structures collected from depths of 20 m and below is consistent with the hypothesis that microbialite biosignature formation is driven by light levels. The occurrence of 13Cenrichment necessitates that photosynthetic drawdown of 12C from the DIC pool outpaces inputs of 13C-depleted (or 12Cenriched) carbon from heterotrophic respiration, implying that

photosynthetic activity is the highest in zones of observed 13Cenrichment. This interpretation is supported by field pulse amplitude modulation (PAM) fluorometry performed in situ on Pavilion microbialites that indicated that microbialite sides tended to receive approximately 25% of the light received by the apex of the structure (PLRP unpublished data). Therefore, the extent of 13C-enrichment along the sides of these microbialites may reflect the variations in exposure to light experienced at different points based on the orientation of the structure. For example, surfaces facing outward from the shore slope or upslope may receive greater light exposure. Therefore, the area where photosynthesis dominates, and high δ13Ccarb values are measured, may be more extensive or widespread. E

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Figure 5. Carbon isotope composition of interior carbonate samples collected from structures located at 10 (A), 18 (B), and 21/26/27 (C) m depth. Here, representative examples selected from multiple profiles taken at each site that best demonstrated trends in δ13Ccarb values from 13Cenrichment near the exterior surface to within the equilibrium range are reported.

Based on these data, an estimate of the area of 13C-enrichment on each microbialite sampled is shown by shaded zones in Figure 4. A trend toward lower δ13Ccarb values with increasing distance away from the apex and toward the SWI was consistent with increased heterotrophic activity and inputs of 13C-depleted DIC. However, no heterotrophic biosignatures (i.e., δ13Ccarb values below the predicted equilibrium zone) were discernible. Because photosynthetic effects can not only result in δ13Ccarb biosignatures, but also increased pH resulting in promotion of carbonate precipitation,13 the corollary to these observations is that microbialite growth rates should be the highest at the apex

and/or exposed surfaces of the structures. Different growth rates of the Pavilion Lake structures were originally hypothesized to be the cause of the variable morphologies of microbialites observed within the lake.23 Within the Pavilion Lake microbialite biofilm, elongated carbonate fabrics attributed to cyanobacteria are oriented perpendicular to the microbialite surfaces23 as would be the case if photosynthetic microbes are oriented to achieve maximum exposure to incoming photosynthetically active radiation (PAR). Further, Theisen and colleagues24 observed that the carbonate micrite crust was thickest on microbialite tops and thinned down the sides, suggesting increased accretion at the apex.24 These F

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exchange with the bulk lake water. Carbonate derived from this source would be expected to have a mean value of −0.6‰.30 In contrast, the most isotopically depleted endmember can be assumed to be inputs of 13C-depleted carbon from heterotrophic respiration of bulk organic matter (δ13Corg assumed to be ca. −25‰). Based on previously published temperature dependent fractionation factors30,35 and measured temperatures within the lake,14 heterotrophically derived secondary carbonate was thus assumed to have a δ13Ccarb value of −14‰. An isotopic mass balance (eq 1) was used to assess the amount of carbonate needed to precipitate from either bulk lake water DIC or heterotrophically 13C-depleted DIC to mask surface biosignatures of photosynthetic origin. Interior δ13C values (δ13Cinterior) will reflect an isotopic mass balance between the fraction of secondary carbonate precipitated (δ13Csecondary, Term 1 in eq 1) and the fraction of primary carbonate originally generated at the surface (δ13Cprimary, Term 2 in eq 1).

results were also consistent with the previously proposed hypothesis that the shallow microbialites, with a greater PAR exposure from multiple angles, have less structured morphologies (i.e., more rounded) and are much more friable due to higher rates of precipitation in all directions.14 Loss of 13C-Enrichment within Microbialite Interior and Obstacles to Preservation. For the microbialites growing at or above 21 m depth, where isotopically enriched nonequilibrium δ13Ccarb values of surface carbonate were observed, results of the intramicrobialite sampling indicated that this signature persisted a maximum of 2 cm below the microbialite surface (Figure 5). Based on previous Δ14C investigations of microbialite carbonate in Pavilion Lake, estimated microbialite growth rates of the past 1000 years were approximately 0.012−0.25 mm/year31 (Brady unpublished data). Assuming these growth rates apply to these samples equally and carbonate continues to accrete at the exterior surface, this implies that the primary surface 13C-enrichment signature is lost in a time frame of 20−400 years. While the observed variation in δ13Ccarb values might be proposed to be recording changes in the DIC of Pavilion Lake over the calculated 20- to 400-year interval, this explanation is not the most likely one. The prevailing environmental and climatic conditions in the Pavilion Lake region are not expected to have varied greatly over this time period. Furthermore, the limestone underlying Pavilion Lake would be expected to buffer against significant changes to the DIC. Both factors imply that there should have been minimal changes in the δ13C value of the DIC system in Pavilion Lake. The more likely explanation for the loss of the surface δ13C biosignature is secondary carbonate precipitation that masks the primary photosynthetic biosignatures. Heterotrophic decay beneath the surface is known to degrade microbial filaments to create vacant pores within the Pavilion Lake microbialite carbonate matrix that are susceptible to carbonate infilling.24,25 Void spaces surrounding primary 13C-enriched carbonate may be infilled with secondary carbonates with δ13Ccarb values controlled by the δ13C of the DIC of the microbialite porewater. Because this porewater may have a different δ13C value than the photosynthetically 13C-enriched DIC from which the carbonate originally precipitated, the secondary carbonate precipitated from it would be added to the primary carbonate and act to mask the photosynthetic biosignature. Impacts of infilling on microbialite morphological features and isotopic composition have been noted in other environments. Dissolution and reprecipitation processes that alter internal fabrics have been noted within Bahamian microbialites32 as have effects on primary laminae grain texture due to the activity of microboring endolithic cyanobacteria.33 The preservation of isotopic biosignatures may have been prohibited as a result of these processes. Microbialites within Storr’s Lake, The Bahamas that exhibit photosynthetic 13Cenrichment of carbonates within primary laminae do not retain this biosignature within the interior of the structures. Instead, primary laminae are altered via heterotrophic processes, and δ13C values become more negative as new carbonate is accreted.34 The δ13CDIC value of the microbialite porewater from which secondary carbonate is precipitating can be assumed to be controlled by two end-member sources. The most isotopically enriched source can be assumed to be the bulk lake water DIC (δ13CDIC value ranges −1.9 to −1.1‰, mean −1.6‰) if microbialite hydraulic conductivity is high and enabling rapid

δ13Cinterior = F(δ13Csecondary ) + (1 − F)(δ13Cprimary )

(1)

Here, F represents the fraction of total carbonate needed to precipitate from porewater DIC to shift the δ13Cinterior value into the predicated equilibrium range. δ13Cprimary is the isotopic composition of the initially precipitated 13C-enriched carbonate. To generate the estimates, the δ13Cprimary value was set at multiple discrete example values that span the range of measured δ13Cprimary values across all samples (Table 1). Table 1. Estimates of Minimum Percent of Secondary Carbonate Required to Mask Primary Photosynthetic Biosignature (e.g. δ13Cinterior = +1.1‰) if Derived from One of Two Potential End-Member Sources: Carbonate from Equilibrium-Based Bulk Lake DIC (δ13Ccarb = −0.6‰) or Heterotrophically 13C-Depleted Carbonate (δ13Ccarb = −14‰)a end-member secondary carbonate sources (%) primary photosynthetic biosignature (‰ VPDB)

bulk lake DIC

heterotrophically altered DIC

3.5 3.0 2.5 2.0 1.5

59 53 45 35 19

14 11 9 6 3

a

Representative photosynthetic biosignature values were used that reflect the range of nonequilibrium δ13Ccarb values observed in Pavilion Lake.

δ13Csecondary values represent the isotopic composition of the secondary (infilling carbonate) which was set to represent the two potential endmember sources (1) derived from bulk lake DIC (δ13CDIC = −1.6‰, therefore mean expected δ13Ccarb value = −0.6‰, Table S1) or (2) heterotrophic inputs to DIC (estimated δ13Ccarb = −14 ‰). eq 1 was solved for F (fraction of secondary carbonate) required to be mixed with δ13Cprimary such that the δ13Cinterior had a δ13Ccarb value of +1.1‰ (minimum shift required) and thus fell within the range of δ13Ccarb values estimated for equilibrium precipitation from lakewater DIC (δ13Ccarb values of −1.5 to +1.1‰13). Based on these estimates, the highest δ13Cprimary carbonate signature (+3.5‰) would be masked by the precipitation of 59% of total carbonate derived from bulk lake water DIC or by 14% of total carbonate being precipitated from heterotrophically derived G

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DIC sources (Table 1). Lower inputs are required to mask signatures that are not as highly 13C-enriched. Because the δ13C value of porewater cannot be determined, it was not possible to differentiate between these end member possibilities, and the occurrence of a mixture of these processes is perhaps most likely. In either case, the relatively short time frame estimated for biosignature preservation in this microbialite system suggests that identification of primary biosignatures within ancient stromatolite associated carbonates may prove challenging.

Allyson L. Brady: 0000-0003-0893-5532 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Thank you to the members of the Pavilion Lake Research Project, with particular mention to Mike Delaney for his management and assistance with SCUBA-based sample collections. Thank you to Martin Knyf for his invaluable assistance in laboratory analyses. Extended thanks to the Ts’Kw’aylaxw First Nation, Linda and Mickey Macri and the Pavilion Community, and British Columbia Parks for their continued support of our research. This work was supported by the Natural Sciences and Engineering Research Council (NSERC) of Canada, and the NASA Mars and Moons Analog Missions Activities (MMAMA). We thank two reviewers for helpful comments that improved the manuscript.

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CONCLUSIONS Biosignatures of photosynthetic origin present on microbialites collected from depths of 20 m and below in both the Central and South Basin of Pavilion Lake were typically localized at the structure apex. While previous studies suggested that δ13Ccarb values higher than isotopic equilibrium were restricted to shallow structures as a result of changing light levels, it was unclear how widely distributed these biosignatures were within the lake itself or on the surface of an individual structure. The 13 C-enriched nonequilibrium δ13Ccarb values measured in the current study are consistent with higher relative amounts of PAR at the apex and a gradual decrease in light exposure, and corresponding photosynthetic activity, on the sides and toward the base of the structure. This decrease in photosynthetic activity, expected increased in heterotrophic activity, and associated inputs of 13C-depleted carbon limits the development of observable 13C-enriched carbonate over the surface of the deeper structures. Within microbialites that exhibited a photosynthetic biosignature associated with surface nodules and biofilms, the 13 C-enriched nonequilibrium δ13Ccarb values did not persist throughout the interior of the microbialites. Instead, the isotopic enrichment was observed to depths of ∼0.5−2 cm below the surface, after which point δ13Ccarb values generally fluctuated within the predicted equilibrium δ13C value range. Loss of 13C-enriched biosignatures is thought to result from deposits of isotopically lighter carbonate from secondary infilling masking photosynthetic 13C-enrichments. Secondary carbonates derived from isotopic equilibrium and heterotrophically 13C-depleted DIC compositions were estimated to mask the maximum observed 13C-enrichments via contributions to total carbonate of ∼59 and ∼14%, respectively. The lack of observable heterotrophic biosignatures suggests that constraining life within the geologic record can be difficult if competing biological isotope effects average to abiogenic standards. Biosignature preservation was estimated to be on the order of 20−400 years, suggesting that isotopic biosignatures in modern microbialite systems are geologically short-lived and potentially of limited value as a tool for interpreting ancient life.

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S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsearthspacechem.8b00182. Table S1: measured DIC δ13C values (PDF)

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DOI: 10.1021/acsearthspacechem.8b00182 ACS Earth Space Chem. XXXX, XXX, XXX−XXX

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DOI: 10.1021/acsearthspacechem.8b00182 ACS Earth Space Chem. XXXX, XXX, XXX−XXX