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Jun 21, 2012 - Stromatolites, consisting mainly of hydromagnesite, are abundant in this lake. The Mg isotope composition of incoming streams, groundwaters, ...
Aquat Geochem (2013) 19:1–24 DOI 10.1007/s10498-012-9174-3 ORIGINAL PAPER

Using Mg Isotopes to Trace Cyanobacterially Mediated Magnesium Carbonate Precipitation in Alkaline Lakes Liudmila S. Shirokova • Vasileios Mavromatis • Irina A. Bundeleva Oleg S. Pokrovsky • Pascale Be´ne´zeth • Emmanuelle Ge´rard • Christopher R. Pearce • Eric H. Oelkers



Received: 7 February 2012 / Accepted: 5 June 2012 / Published online: 21 June 2012 Ó Springer Science+Business Media B.V. 2012

Abstract This study assesses the potential use of Mg isotopes to trace Mg carbonate precipitation in natural waters. Salda Lake (SW Turkey) was chosen for this study because it is one of the few modern environments where hydrous Mg carbonates are the dominant precipitating minerals. Stromatolites, consisting mainly of hydromagnesite, are abundant in this lake. The Mg isotope composition of incoming streams, groundwaters, lake waters, stromatolites, and hydromagnesite-rich sediments were measured. Because Salda Lake is located in a closed basin, mass balance requires that the Mg isotopic offset between Lake Salda water and precipitated hydromagnesite be comparable to the corresponding offset between Salda Lake and its water inputs. This is consistent with observations; a d26Mg offset of 0.8–1.4 % is observed between Salda Lake water and it is the incoming streams and groundwaters, and precipitated hydromagnesite has a d26Mg 0.9–1.1 % more negative than its corresponding fluid phase. This isotopic offset also matches closely that measured Electronic supplementary material The online version of this article (doi:10.1007/s10498-012-9174-3) contains supplementary material, which is available to authorized users. L. S. Shirokova  V. Mavromatis  I. A. Bundeleva  O. S. Pokrovsky  P. Be´ne´zeth  E. H. Oelkers (&) Geoscience and Environment Toulouse (GET), CNRS, UMR 5563, Observatoire Midi-Pyre´ne´es, 14 Avenue Edouard Belin, 31400 Toulouse, France e-mail: [email protected]; [email protected] L. S. Shirokova  O. S. Pokrovsky Institute of Ecological Problems of the North, 23 Nab. Sev. Dviny, Russian Academy of Science, Arkhangelsk, Russia I. A. Bundeleva  E. Ge´rard Equipe ge´obiosphe`re actuelle et primitive, UMR CNRS 7154, Institut de Physique du Globe de Paris, 1 rue Jussieu, 75238 Paris, France C. R. Pearce Department of Earth and Environmental Sciences, The Open University, Walton Hall, Milton Keynes MK7 6AA, UK E. H. Oelkers University of Iceland, Sturlugata 7, 101 Reykjavik, Iceland

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in the laboratory during both biotic and abiotic hydrous Mg carbonate precipitation by cyanobacteria (Mavromatis, V., Pearce, C., Shirokova, L. S., Bundeleva, I. A., Pokrovsky, O. S., Benezeth, P. and Oelkers, E.H.: Magnesium isotope fractionation during inorganic and cyanobacteria-induced hydrous magnesium carbonate precipitation, Geochim. Cosmochim. Acta, 2012a. 76, 161–174). Batch reactor experiments performed in the presence of Salda Lake cyanobacteria and stromatolites resulted in the precipitation of dypingite (Mg5(CO3)4(OH)25(H2O)) and hydromagnesite (Mg5(CO3)4(OH)24H2O) with morphological features similar to those of natural samples. Concurrent abiotic control experiments did not exhibit carbonate precipitation demonstrating the critical role of cyanobacteria in the precipitation process. Keywords Magnesium isotope fractionation  Hydromagnesite precipitation  Alkaline lakes

1 Introduction The fractionation of traditional stable isotopes including C, O, N, S, and B between solids and associated fluids has been used extensively to quantify biogeochemical processes and paleo-environmental conditions in both aquatic lacustrine and marine environments (e.g., Mavromatis et al. 2012b; Pentecost and Spiro 1990; Peterson and Fry 1987). More recently, the fractionation of ‘‘non-traditional’’ stable isotopes of metals such as Ca, Cu, Fe, Li, Mg, and Zn have been applied to illuminating the processes operating in these systems. Of the non-traditional isotope systems, Mg is of particular interest because (1) it is often a major component of lake waters; (2) it is an important component of chlorophyll in aquatic microorganisms (Black et al. 2006, 2007); (3) hydrous Mg carbonate minerals form in lake sediments (Castanier et al. 1993; Power et al. 2009), and (4) stable Mg isotopes fractionate more significantly compared to other alkaline earth metals such as Ca and Sr (Galy et al. 2002; Tipper et al. 2006; Higgins and Schrag 2010; Li et al. 2011; Schauble 2011). The interest in the behaviour of Mg in aquatic systems has been further stimulated by the discovery of Mg carbonates on the Martian surface, which may provide evidence for the presence of Mg-rich waters (Calvin et al. 1994; Russell et al. 1999; Edwards et al. 2005; Palomba et al. 2009). One of the most important processes controlling Mg biogeochemical cycling in continental waters is carbonate biomineralization (Lowenstum and Weiner 1989; Dove 2010). Cyanobacteria-induced mineralization has occurred in lacustrine environments since the Precambrian (Kempe and Kazmierczak 1990; Knoll et al. 1993; Brady et al. 2009; Planavsky et al. 2009; Raven and Giordano 2009; Riding 2000; Ries 2010). Most modern freshwater cyanobacteria-dominated carbonate formation is observed in alkaline environments with high Ca to Mg ratios (Scholl and Taft 1964; Mu¨ller et al. 1972; Otsuki and Wetzel 1974; Kelts and Hsu 1978; Pentecost 1978; Stabel 1986; Thompson and Ferris 1990; Pedone and Folk 1996; Ferris et al. 1997; Thompson et al. 1997; Kazmierczak and Kempe 2006; Dupraz et al. 2009; Power et al. 2011) and produces various Ca-rich carbonate minerals. In contrast, the formation of Mg-rich carbonate minerals by cyanobacteria occurs only in specific Earth surface environments, such as Salda Lake in Turkey, which is fed by ultramafic rock weathering products (e.g., Schmid 1987; Braithwaite and Zedef 1994), alkaline lakes such as those in British Columbia (Renault 1990; Power et al. 2007, 2009), and in some saline lake sediments (Renaut and Long 1989; Renaut and Stead 1990; Queralt et al. 1997).

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In contrast to our detailed understanding of Ca-bearing carbonate mineral precipitation associated with cyanobacterial activity (Jørgensen and Revsbech 1983; Cox et al. 1989; Merz 1992; Hartley et al. 1995, 1996; Obst and Dittrich 2006; Obst et al. 2009; Dittrich and Sibler 2010; Kranz et al. 2010), the factors controlling hydrous Mg carbonate mineral precipitation and stable Mg isotope fractionation in natural waters are still poorly constrained (i.e., Mavromatis et al. 2012a). Salda Lake, located in SW Turkey, is an ideal natural laboratory where contemporary Mg carbonate precipitation can be studied to overcome this knowledge gap. Previous studies provide information on the geology, hydrology, chemistry, biology, and mineral formation processes occurring in the Salda Lake basin (e.g., Braithwaite and Zedef 1994, 1996). These previous studies suggest that most of the hydromagnesite (Mg5(CO3)4(OH)24H2O) stromatolites developed along the Salda Lake coast were formed by cyanobacterial and algal activity (Braithwaite and Zedef 1994). In this study, we sampled Salda Lake waters, sediments, and stromatolites and performed laboratory experiments to characterize the magnitude and mechanisms of stable Mg isotope fractionation occurring during Mg carbonate precipitation. Results of this study are the first quantitative calibration of Mg isotope fractionation between aqueous solutions and naturally formed hydrous Mg carbonates. As such, these results may be useful for tracing biomineralization processes in past and contemporary continental aquatic environments.

2 Materials and Methods 2.1 Site Description Salda Lake (also known as Salda Go¨lu¨ in Turkish) is located in SW Turkey. It has a surface area close to 45 km2 and an average depth of 80 m, with a maximum reported depth of 200 m (see Fig. 1). Its limnology, geology, and geochemistry have been extensively described in the literature (Schmid 1987; Braithwaite and Zedef 1994, 1996; Russell et al. 1999; Zedef et al. 2000; Kazanci et al. 2004). This lake is a natural analog for mineralogic carbon storage (e.g., Oelkers and Schott 2005; Oelkers et al. 2008), as meteoric waters feeding the lake dissolve adjacent ultramafic rocks and precipitate hydromagnesite in shallow littoral zones. A similar process has recently been documented in the British Columbia playas (Power et al. 2009). Salda Lake has no surface outlet, and the lake water level drops up to 1 metre during the summer (our observations and Zedef et al. 2000). As the lake is located at the top of a regional watershed, some water loss through subsurface drainage channels is possible. However, as noted by Russell et al. (1999) and Zedef et al. (2000), the elevated Na concentration of the lake water suggests that evaporation is the dominant Salda Lake water draining process. Based on our field measurements of the surface water inputs to the lake in September and February, we estimate that a total of 1–10 m3/s of water enters the lake. Taking account of this flux, the residence time of Salda Lake water is 10–100 years. The residence time of Mg is longer as the Mg concentration of the lake water exceeds that of the incoming springs by a factor of 3 (see Sect. 3.1.1 below). Contemporary hydromagnesite stromatolites are present in the littoral zone of the SW part of the lake. These stromatolites especially are abundant at the Kocaadalar Burnu site (T 08 in Fig. 1) and form three 20–100 m2 mounds situated *50 m offshore and rise *10 m from the lake bottom, reaching to 3–4 m above of the lake surface. Images of Lake Salda stromatolites are shown in Fig. 2. Similar to Braithwaite and Zedef (1994, 1996), we define all of the

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1477 m T11

T10

1461 m

Salda T12

T07

T08

1472 m T3 T09

T1 T2

N 1402 m

Yesilova

5 km Schematic map of Lake Salda and sampling points Fig. 1 Schematic map of Salda Lake showing locations of samples collected in this study

modern, actively growing microbialite structures as ‘‘stromatolites.’’ Underwater diving examination of the deepest part of these mounds showed no evidence of stromatolites below 6–10 m water depth. Stromatolites 1–1.5 m2 in size were found in other parts of the lake within 10–20 m of the shoreline. Finally, in the littoral zone of the north side of the lake, most of the submerged stones were covered by actively forming, non-solidified stromatolites, such as shown in Fig. 2d. These submerged stones exhibit the same surface appearance as the larger mounds. Detailed underwater examination of the stromatolite surfaces demonstrated that they are alive and actively growing (cf. also Braithwaite and Zedef 1994, 1996). The surfaces of the hydromagnesite comprising the stromatolites were covered by a layer of green algae, diatoms, and cyanobacteria with gas bubbles (presumably oxygen) adjacent to the surface of the microbial mats such as shown in Fig. 2b. 2.2 Lake Water and Mineral Sampling Water samples were collected from inflowing streams and the lake littoral zone in February 2008, February 2010, and September 2010. A profile of the lake water column (down to 70 m depth) was also collected from the middle of the lake in September 2010 using an Aquatic Research Co. horizontal polycarbonate water sampler, enabling ultraclean sampling in the field (Shirokova et al. 2010; Pokrovsky et al. 2012). The water samples were immediately filtered through sterile, single-use Sartorius MinisartÒ 0.45-lm acetate cellulose filters. Dissolved oxygen, pH, and temperature were measured on-site with an

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Fig. 2 Images of the stromatilites observed in this study a modern stromatolite formations in the littoral zone. b The surface of active stromatolite covered by Spyrogyra sp. algae and diatoms with oxygen bubbles illustrating active ongoing photosynthesis. c Underwater images of deep (5 m) massive stromatolites surfaces at the Kocaadalar Burnu site T 08 d stromatolite coatings of the peridote rock debris taken from a depth of 1–1.5 in the littoral zone (sample T 11)

uncertainty of 5 %, 0.02 units, and 0.5 °C, respectively. Concentrations of dissolved organic carbon (DOC), Cl, SO4, alkalinity, cations, and trace elements (TE) were subsequently measured in the laboratory using methods routinely applied for analysis of lake and river water samples (Pokrovsky et al. 2010, 2011b; Shirokova et al. 2010; Vasyukova et al. 2010). Between 2 and 5 l of surface water were also filtered on-site using a sterile Nalgene disposable filter unit and 0.22-lm polycarbonate filters. These samples were stored at 5 °C in sterile polypropylene containers and subsequently used for the bacterial culturing. Hydromagnesite samples were collected from (1) the shallow part of the stromatolite mounds located at Kocaadalar Burnu (within the 0.5–1.0 m of the surface, e.g. Fig. 2a), (2) parts of stromatolites located from 4 to 5 m depth at the same site (e.g., Fig. 2c), and (3) other subaerial stromatolite islands located at the lake littoral (e.g., Fig. 2a, b). We also sampled (1) hydromagnesite sand from the lakeshore, (2) carbonate coatings from submerged branches and grasses, and (3) carbonate coatings from ultramafic rock debris located in the littoral zone (e.g., Fig. 2d). The position of all sampling localities is shown in Fig. 1. 2.3 Cyanobacterial Culture Isolation and Laboratory Experiments A culture of Synechoccocus sp. cyanobacteria was isolated from the surface of stromatolites sampled in February 2008 from the depth of 1 m at 50 m from the Salda Lake shoreline. The culture was purified on agar BG-11 or Pratt media (cf. Martinez et al. 2008

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for chemical composition) and individual colonies were grown in synthetic, cyanobacteria BG-11 Freshwater Solution for 3 weeks under continuous fluorescent light of 2000 lux until the stationary growth phase was attained. Cyanobacterium Synechoccocus typically consists of isolated elongated cells without significant mucilage as evidenced from optical microscope and TEM examination (Shirokova et al. 2011). Phylogenetic attribution of the collected and grown cyanobacterium Synechoccocus was performed by DNA extraction (UltraCleanÒ Microbial DNA Isolation Kit MO BIO) and 16S RNA gene amplifying. The purified culture has 99 % of their 16S RNA genes in common with Synechococcus sp. B8901, a cyanobacterium already reported to occur in alkaline lakes, including Salda Lake (Girgin et al. 2004; Mavromatis et al. 2011). A similar cyanobacterial culture was isolated from the stromatolite interior and from the algal coating collected from submerged branches located in an inflowing stream. As such, this culture can be viewed as representative of the Salda Lake periphyton. Note that other cyanobacterial species like Gloeocapsa sp. were also reported to occur in Salda Lake stromatolites and its water column (Braithwaite and Zedef 1994). The concentration of the bacterial cell suspensions was quantified via optical density (O.D.) using a spectrophotometer at a wavelength of 750 nm (Sarcina and Mullineaux 2000). The O.D.—wet bacterium weight calibration curve was linear up to 1.3 absorbance units, and the ratio between wet and freeze-dried weight of cells was 8.0 ± 2.0. Laboratory experiments were designed to precipitate hydrous Mg carbonates in the presence of (1) the Synechoccocus sp. cultures extracted from the Salda Lake stromatolites and (2) a model Gloecapsa sp. culture extensively studied by our group over the past 5 years (Pokrovsky et al. 2008a, b; Mavromatis et al. 2012a). Experiments were performed in 1,000 ml sterile borosilicate glass reactors. The Synechoccocus sp. experiments were performed using sterile Salda Lake water (0.014 M Mg, 0.03 M Dissolved Inorganic Carbon, DIC) amended with low-phosphate (50 lM or 10 % of its usual content) BG-11 nutrient components (Sigma-Aldrich C3061, Rippka et al. 1979). The Gloeocapsa sp. experiments were performed using an aqueous Mg(HCO3)2 solution containing 0.025 M MgCl2 and 0.05 M NaHCO3, amended with 50 lM phosphate and all BG-11 components. The distinct growth solutions for the Gloeocapsa sp. experiments were chosen to be consistent with the previous experiments (Mavromatis et al. 2012a). A summary of the compositions of all fluids used in the experiments is provided in Table 1 and Table ESM-2 of the Electronic Supplement. Duplicate live culture and control experiments were performed at 25 ± 2 °C. Control experiments were performed in both cell-free media (e.g., S-Abio-3, 5, 6, Table 1) and in nutrient-free aqueous solutions in the presence of non-growing Synechoccocus sp cells (e.g., S-Bio-6, Table 1). Bacteria growth in the experiments was initiated by adding 0.1–0.15 gwet/l of previously grown cyanobacteria rinsed in 0.1 M NaCl solution to the reactors that were continuously stirred at 150 rpm with a magnetic stirring bar without air bubbling. Reactors were open to the atmosphere via BiosilicoÒ silicon porous caps. Each of these experiments was performed under continuous fluorescent light of 3000 lux which is similar that of an overcast day. 2.4 Sampling and Analyses Homogeneous suspensions containing the fluid, precipitated minerals, and cells, if present, 30–50 ml aliquots were sampled periodically from the reactors in a sterile laminar hood box. The optical density and the pH were measured in liquid subsamples, while the fluid supernatants were initially filtered, using 0.22 lm filters, and used for alkalinity, DOC, and Mg concentration measurements. Alkalinity was determined by HCl titration using an

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100

100

Salda Lake water without BG-11

Salda Lake water ? BG-11

BG-11 ? (0.025 M MgCl2 ? 0.036 M NaHCO3)

BG-11 ? (0.025 M MgCl2 ? 0.036 M NaHCO3)

Salda Lake water ? BG-11

Salda Lake water ? BG-11

Salda Lake water ? BG-11

S-BIO-6

S-BIO-7

S-BIO-8a

S-BIO-10

S-ABIO-3

S-ABIO-5

S-ABIO-6

34

0

0

0

0.05–3.5

0.05–4.0

0.2–0.6

0.2–0.9

0.1–3.0

0.2–2.2

Biomass range, gwet/l

9.3–9.4

8.2–9.46

9.2–9.39

8.5–10.8

8.4–10.4

9.4–9.9

9.2–9.6

9.3–10.8

9.2–10.8

pH range

13.1–13.8

21–22

13–12

25–5

25–5

25–5

9.5–12

14–3

15–2.5

Mg concentration range (mM)

a

Gloeocapsa sp. culture

Abiotic experiments were conducted in the presence of 0.01 M NaN3 to avoid any bacterial growth

62

35

35

120

34

36

Salda Lake water ? BG-11

Salda Lake water ? BG-11

S-BIO-3

Experiment duration (days)

S-BIO-4

Initial reactive fluid

Experiment

Table 1 Experimental conditions of all experiments performed in this study

5–8

5–8

7–10

10–40

20–120

5–15

2–5

9–17

7–18

DOC range, mg/l

No precipitation

No precipitation

No precipitation

N.D.

N.D.

N.D.

No precipitation

-0.435

-0.38

Rate mmol l-1 day-1

Hydromagnesite

Hydromagnesite

Hydromagnesite, dypingite

Dypingite, hydromagnesite

Dypingite, hydromagnesite

Solid phase

Aquat Geochem (2013) 19:1–24 7

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automatic Schott TitroLine alpha TA10plus titrator with an uncertainty of ±2 % and a detection limit of 5 9 10-5 M. The DOC content was determined using a Shimadzu TOC6000 SCN Carbon Total Analyzer with an uncertainty of 3 % and a detection limit of 40 9 10-6 M. Magnesium concentrations were measured by flame atomic absorption spectroscopy using a Perkin Elmer AAnalyst 400 with an uncertainty of ±2 % and a detection limit of 0.2 9 10-6 M. pH was measured using a Mettler Toledo combined electrode, with a precision of ±0.01 units. The uncertainty of biomass concentration determination via optical density is estimated to be ±10 %. Prior to sample characterization by scanning electron microscopy (SEM), organic matter was removed from the solid phases by treating them in aqueous 10 % H2O2 for 2–3 days at the same pH, DIC, and Mg concentrations as used in the experimental fluids. The residual solids were then thoroughly rinsed with de-ionized water and freeze-dried at -55 °C. The mineral phases were then characterized using a JEOL JSM840a SEM, and an INEL CPS 120 X-ray diffractometer using Coja, with a scan speed of 0.02 s-1. Untreated solids were kept for chemical analysis as described below. 2.5 Magnesium Isotope Analyses The Mg isotope compositions of selected liquid and solid samples were analysed according to the procedure described by Pokrovsky et al. (2011a). Magnesium isotopic ratios were measured using a Thermo-Finnigan ‘‘Neptune’’ Multi Collector Inductively Coupled Plasma Mass Spectrometer (MC-ICP-MS) at the GET (Toulouse, France) and at The Open University (Milton Keynes, UK). Instrumental mass fractionation effects were corrected via sample-standard bracketing, and all results are presented in delta notation with respect to the DSM-3 international reference material (Galy et al. 2001; Goldstein et al. 2003): 0 x  1 Mg

24

B Mg sample C  1A  1000 d Mg ¼ @  x  x

Mg

24 Mg

ð1Þ

DSM3

where x refers to the Mg mass of interest. The reproducibility of d26Mg analyses was typically \0.08 % as confirmed by replicate analyses of three international Mg reference standards (DSM-3, CAM-1 and OUMg). The enrichment factor between the Mg in the fluid and that incorporated into the solid phase is defined as: D26 Mgsolidliquid  d26 Mgsolid  d26 Mgliquid

ð2Þ

This value was determined for all samples where coexisting fluid and solid phases were collected in the present study.

3 Results 3.1 Chemical and Mg Isotopic Composition of Salda Lake Water and Minerals 3.1.1 Hydrochemistry The major and trace element compositions of all collected natural samples are listed in the Electronic Supplement (Table ESM-1). The Mg concentration, alkalinity, and pH

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measured in Salda Lake waters and inflowing streams are consistent with values reported by Braithwaite and Zedef (1994, 1996) and Kazanci et al. (2004). In February 2008 and February 2010, the surface water temperature was 8–10 °C, whereas in September 2010, it varied from 27.5 °C at the surface to 13 °C at 70 m depth. The fastest stromatolite growth occurs in warm water at high solar radiation during the summer (Braithwaite and Zedef 1996). As such, detailed chemical and isotopic analysis of the lake water composition was performed on samples collected during September 2010 when the water temperature was highest. At this time, pH decreased from 9.15 at the surface to 9.03 at the bottom of the water column; DOC concentrations ranged from 4.1 to 3.6 mg/l, while alkalinity and Mg, Ca, and Cl concentrations remained constant in the water column and were equal to 0.032 ± 0.001 M, 390 ± 5, 4.0 ± 0.1, and 195 ± 5 mg/l, respectively. The Mg and DIC concentration of incoming streams and groundwaters was *3 times lower than that of the lake water, although there were significant variations between the individual samples (from 70 to 120 mg/l for Mg and from 0.07 to 0.02 M for Alk).

3.1.2 Stromatolite Mineralogy The examined stromatolites were dominated by hydromagnesite, as shown by XRD analysis of multiple spots of a 20-cm-thick representative sample and littoral sediments. The carbonate sand collected from the littoral zone was also composed of hydromagnesite as it originated from the wave abrasion of the stromatolites (Braithwaite and Zedef 1996). The external stromatolite surface was covered with rosettes of hydromagnesite 10–20 lm in diameter (c.e. Fig. 3a, b) and often exhibited a honeycomb-like structure as revealed by SEM observations (c.e. Fig. 3c, d). Platelets of hydromagnesite are evident in the inner parts of stromatolites, which were not exposed directly to lake water (c.e. Fig. 3f). The interior of stromatolites were comprised of 4–8-lm-diameter spheres (c.e. Fig. 3e) made of hydromagnesite platelets (c.e. Fig. 3f). These crystal forms were commonly observed and are abundant in all investigated hydromagnesite samples. Imprints of Spyrogyra sp. green algae identified by optical microscope examination were often recognized on stromatolite surfaces by SEM analysis (not shown) as these algae efficiently colonized stromatolite surfaces forming visible oxygen bubbles (c.e. Fig. 2b).

3.1.3 Mg isotopes in Salda Lake Water and Mg Carbonate Stromatolites The d26Mg composition of selected sampled waters is listed in Table 2. The Mg composition of the water column was homogeneous at the time of sampling (September 2010) and did not vary between different sites in the littoral zone or due to the presence of stromatolites (see Table 2). The mean d26Mg composition of the water column in September 2010 was 0.12 ± 0.04 %. This is somewhat more positive than at the other sampling times; the mean d26Mg composition of the water was found to be -0.02 and -0.01 % in February 2008 and February 2010, respectively, probably due to higher carbonate mineral precipitation during the summer months. Lake water samples have d26Mg compositions 0.8–0.9 % more negative than seawater (Hippler et al. 2009; Foster et al. 2010). The incoming spring and ground waters had distinctively lighter d26Mg compositions ranging between -1.40 and -0.80 %; these values are within the range of major riverine systems (Tipper et al. 2006). The internal and external parts of stromatolites and the littoral sand exhibited a range of d26Mg from -1.04 to -0.94 %.

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Fig. 3 SEM images of natural stromatolites collected from Salda Lake. a, b External surfaces of stromatolites from the coastal zone, collected at Kocaadalar Burnu (sample T 08). c, d The massive stromatolite mounds and subaerial stromatolite islands of T3, and e, f interior part of the stromatolite T 08

3.2 Hydrous Mg Carbonate Precipitation Experiments The measured chemical composition of the reactive fluids and the mineralogy of precipitated solid phases of all experiments are listed in the Table ESM-2 of the Electronic Supplement. The X-ray patterns of precipitated Mg carbonates are presented in Fig. ESM-1 of the Electronic Supplement. 3.2.1 Solid Phases X-ray diffraction analysis demonstrated the precipitation of dypingite (Mg5(CO3)4(OH)2 5H2O) and often hydromagnesite (Mg5(CO3)4(OH)24H2O) at distinct times in some of the

123

0.14 ± 0.06

0.08 ± 0.01

Samples were collected during September 2010 unless otherwise noted

-0.02 ± 0.05

-0.38 ± 0.05

Site T 1: coastal lake water, Feb 2008

Site T 2: incoming spring, Feb 2008

-0.76 ± 0.03

-0.01 ± 0.07

-1.01 ± 0.11

-1.4 ± 0.05

-0.73 ± 0.04

-0.54 ± 0.10

Site T 09: incoming spring

0.08 ± 0.04

0.17 ± 0.03

0.05 ± 0.02

Site T 10: spring under mountain

Site T 11: 1.5 m depth, fragm. stromatolites

Site T 07—at a depth of 70 m

0.12 ± 0.08

0.10 ± 0.03 0.04 ± 0.03

Site T 07—at a depth of 40 m

Site T 07—at a depth of 60 m

0.09 ± 0.05

0.08 ± 0.02 0.04 ± 0.04

0.15 ± 0.01

-0.02 ± 0.01

Site T 07—at a depth of 0 m

-0.001 ± 0.01

0.08 ± 0.03

0.05 ± 0.02

0.26 ± 0.07 -0.14 ± 0.15

-0.06 ± 0.08

0.13 ± 0.02

-0.40 ± 0.03

-0.48 ± 0.01

-0.53 ± 0.04

-0.50 ± 0.07

-0.36 ± 0.05

d25Mg

d25Mg

d26Mg

Mineral samples

Fluid samples

Site T 07—at a depth of 20 m

Lake depth profile:

Site T-09 live stromatolites

Site T-08: Salda-Wate Feb 2010

Site T 08: stromatolite—exterior part

Site T 08: stromatolite—interior part

Coastal water and carbonate sediments

Site T 3: Salda Lake coast and stromatholites

Sample description

Table 2 Mg isotopic composition of natural samples measured in the present study

-0.75 ± 0.02

-0.94 ± 0.02

-1.04 ± 0.03

-0.99 ± 0.15

-0.7 ± 0.04

d26Mg

-1.02

-1.12

-0.86

-0.95

D26Mg solid–fluid

Hydromagnesite

Hydromagnesite

Hydromagnesite

Hydromagnesite

Mineralogy

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Fig. 4 SEM images of laboratory precipitates. a–c Hydromagnesite and dypingite from experiment S-Bio-7; d hydromagnesite/dypingite of experiment S-Bio-3; e hydromagensite of experiment S-Bio-8; f optical microscope photo of mineral-free suspension of Gloeocapsa sp. cyanobacteria

experiments. SEM images revealed that the dypingite was present as 2–10-lm-diameter aggregates that grow with time to 5–15-lm rosettes (e.g., Fig. 4 a–c). Hydromagnesite was commonly observed to precipitate as 5–10-lm rosettes of flat crystals (e.g., Fig. 4d). The rosette-like dypingite and hydromagnesite aggregates obtained in experiments with growing Synechoccocus sp. cyanobacteria during experiment S-Bio-7 and S-Bio-3 (e.g., Fig. 4b, d) were similar to the natural hydromagnesite of external stromatolite surfaces (e.g., Fig. 3a). The hydromagnesite crystals formed from the experiment containing Gloeocapsa sp. cyanobacteria (e.g., Fig. 4e) during experiment S-Bio-8 exhibit similar morphology to the external surface of Salda Lake stromatolites (e.g., Fig. 3c, d). The embedding of cells and

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cell associates was evident in experiment S-Bio-8 (e.g., Fig. 4f) and was likely responsible for the honeycomb structure of Mg hydrous carbonates formed in the presence of cyanobacteria (e.g., Fig. 4e) as well as in natural stromatolites (e.g., Fig. 3c). 3.2.2 Chemical Composition of the Fluid Phase The temporal evolution of pH and Mg concentration in all experiments as well as the temporal evolution of alkalinity and biomass concentrations during biotic and abiotic experiments are illustrated in Fig. 5. The Mg concentration and alkalinity of the reactive fluids tended to decrease and the pH tended to increase with time during all bacteria, nutrient-present experiments. Abiotic experiments did not produce a measurable decrease in Mg concentration or alkalinity, although a slight pH increase was observed. The addition of BG-11 nutrient components to Salda Lake water had a significant effect on biomass production (e.g., Fig. 6) and Mg hydrous carbonate precipitation, as evident from the decrease in Mg concentration (e.g., Fig. 5b). The mass of precipitated hydrous magnesium carbonate is plotted as a function of the biomass present in the reactor fluid in Fig. 7. The line drawn in this figure consistent with the results of all experiments containing biomass can be described by: Mgprecipitated ðmmoles) = (6:0  0:25Þ  Biomassproduced ðgwet Þ;

R2 ¼ 0:81

ð3Þ

Converting this relationship into molar scale and noting that (1) the ratio of wet-to-dry biomass of Synechoccocus sp. is 8 ± 2 and (2) that the proportion of carbon in dry biomass is 50 % indicates that the molar inorganic Mg to organic C ratio in the biotic experiments is 1.17 ± 0.1. This value is consistent with the following reaction coupling hydromagnesite precipitation with cyanobacterial photosynthesis in aqueous Mg(HCO3)2 solutions: 5Mg2þ þ 10HCO 3 ¼ 6H2 O = Mg5 ðCO3 Þ4 ðOH)2  4H2 O # + 6CH2 O + 6O2 "

ð4Þ

The speciation and saturation state of the reactive fluids with respect to potentially precipitating mineral phases for all experiments was calculated using PHREEQC software (v.2.17.4799) together with its MINTEQA2 database (Parkhurst and Appelo 1999) after adding to it thermodynamic properties for nesquehonite and hydromagnesite reported by

A

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4 2

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Elapsed time, days

80

0

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Fig. 5 Temporal evolution of pH (a) and Mg concentration (b) during selected experiments. The symbol size encompasses the uncertainty of analyses. The lines connecting the data points are for the aid of the reader

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Biomass, gwet/L

Fig. 6 The temporal evolution in biomass evolution during experiments performed in experiments preformed in bacteria-present, nutrient-present experiments (experiments S-Bio3 and S-Bio-4, circles and diamonds) and in the bacteriapresent, nutrient-free experiment (S-Bio-6). The lines connecting the data points are for the aid of the reader

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1.5

1.0

S-Bio-4

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S-Bio-3

S-Bio-6

0.0

0

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40

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Elapsed time, days 16 14 12

Delta [Mg], mM

Fig. 7 The mass of magnesium precipitated as a function of the corresponding increase in biomass (gwet) during experiments S-Bio-3 and S-Bio4. The solid line represents a linear least squared fit of these data with a correlation coefficient, R2 = 0.81

10 8 6

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S-Bio-4

2 0

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Biomass increase, g wet /L

Cheng and Li (2010a, b). The speciation of aqueous Mg during the experiments was dominated by aqueous Mg2?, but also contained significant concentrations of MgCO3-(aq) and MgHCO03. Note that aqueous Mg2? complexation with organic ligands not present in the thermodynamic databases such as cyanobacterial exometabolites, soluble EPS, and siderophores is unlikely to be significant, as the Mg to organic ligand ratios of all fluids was [10. The evolution of the saturation state of the reactive fluids with respect to nesquehonite and hydromagnesite in biotic and abiotic experiments is illustrated in Fig. 8a, b, respectively. Other Mg-bearing carbonates were not considered as they were not identified either in Salda Lake waters or in our experiments. The degree of supersaturation of the fluid phase with respect to these two phases (Xnesquehonite, and Xhydromagnesite,) is defined as the ratio of ion activity product, IAP, to the solubility product of the mineral; the latter values were taken from MINTEQA2 database. The saturation state of these fluids with respect to dypingite was not calculated owing to lack of relevant thermodynamic data (cf. Hopkinson et al. 2012).

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S-Bio-3 S-Bio-4

1.0

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0.6 0.4 0.2 0.0

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0.1 0.01

0.001

0

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20

30

40

50

Elapsed time, days Fig. 8 Temporal evolution of the reactive fluid solution saturation with respect to nesquehonite (Xnesquehonite), (a) and hydromagnesite (Xhydromagnesite), (b) during experiments S-Bio-3, S-Bio-4, S-Bio-6, S-Abio-3, and S-ABio-6. Fluids for which Xi [ 1 are supersaturated with respect to the ith mineral, whereas fluids for which Xi \ 1 are undersaturated with respect to the ith mineral. The lines connecting the data points are for the aid of the viewer

The initial saturation state of fluids in the bacteria, nutrient-present experiments with respect to nesquehonite ranged from 0.02 to 0.6, then maximized to 0.7–0.8, before massive mineral precipitation, after which it decreased to &0.2. Note that nesquehonite is commonly the first precipitating phase in the Mg-CO2-H2O system at 25 °C in the presence and absence of cyanobacteria (e.g., Mavromatis et al. 2012a; Hopkinson et al. 2012). Similarly, the saturation state of these fluids with respect to hydromagnesite maximized during the experiments, becoming supersaturated after 5 days, then decreased to *0.1 after *20 days. The bacteria-present, nutrient-free experiment and two abiotic experiments failed to supersaturate with respect to hydromagnesite. This observation is consistent with the lack of hydromagnesite precipitation in these experiments Apparent precipitation rates (ri) in the presence of Synechoccocus sp. were calculated from the first derivative of the fluid phase Mg concentration (cMg) with respect to time (t),

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from the onset of precipitation to the attainment of near constant fluid Mg concentrations using: ri ¼

dcMg : dt

ð5Þ

Apparent rates equal -0.40 ± 0.03 mmol Mg l-1 day-1 and are similar to that reported for dypingite precipitation in the presence of Gloeocapsa sp. during stirred, non-bubbled experiments by Mavromatis et al. (2012a).

4 Discussion 4.1 Comparison of Salda Lake Sediments and Laboratory Precipitates In accordance with the previous studies of Salda Lake stromatolites, the present study confirmed the dominance of hydromagnesite (Mg5(CO3)4(OH)24H2O) in the stromatolites. The external surface of stromatolites had a porous, honeycomb-like structure suggesting the presence of bacterial associates or cyanobacterial colonies. The persistence of hydromagnesite both in the littoral sediments and in live stromatolites confirms its long-term stability in the lake water. This observation agrees with reports of hydromagnesite’s dominance in alkaline playas of British Columbia (Power et al. 2009) and the persistence of hydromagnesite in other alkaline lake sediments (Renaut and Long 1989; Queralt et al. 1997). The saturation indexes of nesquehonite and hydromagnesite are plotted as a function of depth in Fig. 9a, b, respectively. The bottom waters of Salda Lake were undersaturated with respect to nesquehonite. In contrast, surface waters (\5–10 m depth) are supersaturated with respect to nesquehonite and strongly supersaturated with respect to hydromagnesite. This is consistent with occurrences of stromatolites in Salda Lake only above 10 m depth. In contrast, the incoming streams are strongly undersaturated with respect to hydromagnesite (Xhydromagnesite \ 10-3) and nesquehonite (Xnesquehonite B 0.1). These observations suggest the importance of microbial photosynthetic activity in promoting hydromagnesite precipitation by increasing its saturation state; photosynthesis is most important near the lake surface. Moreover, the elevated water temperature near the surface also tends to increase the saturation state of the lake waters with respect to hydromagnesite. A striking similarity was observed between hydrous Mg carbonates forming at the surface of live stromatolites in Salda Lake (e.g., Fig. 3a–d) and those precipitating during laboratory experiments in the presence of Synechoccocus sp. and Gloeocapsa sp. cyanobacteria (e.g., Fig. 4c–e), as well as in numerous field observations reported in the literature (e.g., Fig. 11 in Dupraz et al. 2004). Dupraz et al. (2009) observed that discontinuous exopolysaccharide (EPS) calcification leads to a micropeloidal structure resulting from the presence of coccoid clusters or filamentous bacteria remnants. Furthermore, these authors reported that no CaCO3 precipitation is observed in or on the sheaths of cyanobacteria, and only a negligible precipitation is directly associated with the inner layers of the active filamentous cyanobacteria mats (see also Martinez et al. 2010). Instead, precipitation occurs in the uppermost mat layer, which is composed of EPS, empty filamentous bacteria, and coccoids (e.g., Gloeocapsa spp.). Results of the present study corroborate a mechanism of honeycomb-like structure formation via hydrous Mg carbonate precipitation due to the presence of EPS and cell capsules.

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Ω Nesquehonite 0

0.5

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Depth, m

Fig. 9 The saturation index of nesquehonite (a) and hydromagnesite (b) in Salda Lake water at T07 station (blue diamonds) and coastal stromatolite settings (pink squares) as a function of depth. The incoming streams are strongly undersaturated with respect to both nesquehonite and hydromagnesite (B0.1 and \103, respectively)

17

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B

100

1000

10000

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10

Depth, m

20 30 40 50 60 70 80

The amount of precipitated hydrous Mg carbonate and biomass production were highly correlated (R2 * 0.8) in our laboratory experiments, which is consistent with theoretical mineral yield during the biomass production (e.g., Fig. 7). Given the similarity of aqueous fluid compositions in the experiments and in Salda Lake, we suggest that the linear relationship shown in Fig. 7, consistent with Eq. 4, can be used to predict quantitatively the amount of hydrous Mg carbonate precipitation in the presence of photosynthesizing cyanobacteria in aquatic environments dominated by the precipitation of this mineral.

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4.2 The Mechanisms of Mg Carbonate Precipitation in the Presence of Cyanobacteria Carbonate mineral formation in the presence of photosynthetic bacteria has been attributed to the alkaline environment produced by hydroxyl ion release stemming from photosynthesis (Thompson and Ferris 1990; Douglas and Beveridge 1998). pH was observed to increase in all experiments performed in this study, although this increase was small in the abiotic experiments and the bacteria-present, nutrient-free experiment. In all experiments, slight initial pH increases originated from the degassing of the initial reactive fluid which contained 3–5 9 10-2 mol/kg NaHCO3 at pH * 8.2–9.2. Owing to this high aqueous bicarbonate concentration, these initial fluids had a pCO2 of *(0.3–10) 9 10-2.0 atm, which is supersaturated with respect to the atmosphere. In the bacteria-present, nutrientpresent experiments, this pCO2 decrease was accompanied by an additional pH increase due to photosynthetic uptake of HCO3- ions and OH- release. During the bacteria-present, nutrient-present experiments, strong supersaturation likely occurs in the vicinity of cells during photosynthesis (e.g., Pokrovsky and Savenko 1995). Significant supersaturation, due to a local pH increases, in microbial mats has been previously reported by Jørgensen and Revsbech (1983) and Shiraishi et al. (2008). Whereas the bulk supersaturation increase is clearly visible in the temporal evolution of the hydromagnesite saturation state (c.e. Fig. 8b), the local supersaturation in the vicinity of live cells could be much higher, sufficient for the precipitation of nesquehonite as a precursor phase. The absence of Mg carbonate precipitation in abiotic and nutrient-free biotic experiments, therefore, likely stems from the insufficient fluid supersaturation with respect to hydromagnesite due to the lack of photosynthetically induced pH rise. In addition, the absence of bacterial cell yields highly homogeneous solutions incapable of triggering the Mg carbonate homogeneous nucleation; carbonate mineral systems require significant supersaturation for precipitation (cf., Pokrovsky 1998). Results of bacterial experiments in the presence of nutrients demonstrate that cyanobacteria increase the bulk solution pH hence increasing the degree of fluid supersaturation with respect to carbonate minerals. Additional literature evidence suggests that these bacteria also provide favourable mineral nucleation sites. The surfaces of the bacteria have been proposed to affect the crystal morphology of carbonate minerals through the chemistry of polysaccharides (e.g., Braissant et al. 2003, 2007; Dittrich and Sibler 2010). The role of cyanobacterial polysaccharides on Mg hydrous carbonate precipitation is confirmed by the similarity of hydrous Mg carbonate crystals observed in natural stromatolites and those grown in laboratory cultures (cf. Figs. 3b, 4c, d). The capacity of a single culture to precipitate carbonate crystals with a similar form as those of microbial consortia of Salda Lake stromatolites may have important consequences on Mg-rich carbonate formation. If the presence of live cyanobacteria is capable of inducing hydromagnesite precipitation simply by increasing pH and supersaturation and without additional action of other bacteria, then the formation of Mg-rich stromatolites in the Precambrian could occur via the simplest life forms, before the emergence of complex microbial consortia. This conclusion questions the hypothesis that the postmortem decomposition of cyanobacterial sheaths by heterotrophic bacteria is responsible for magnesium carbonate precipitation in ancient dendritic reef structures as proposed by Laval et al. (2000). 4.3 Mg Isotope Fractionation During Hydromagnesite Precipitation in the Salda Lake Dypingite precipitated in the presence of Gloeocapsa cyanobacteria exhibit a D26Mgmineral-solution value between -1.4 and -1.25 % (Mavromatis et al. 2012a). The

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preferential incorporation of light Mg isotopes in the precipitating solids is consistent with previous Mg isotope analyses on biogenic skeletal carbonates (e.g., Chang et al. 2004; Buhl et al. 2007; Hippler et al. 2009; Wombacher et al. 2011) and abiotically precipitated low Mg calcite (e.g., Galy et al. 2002; Immenhauser et al. 2010). The isotopic fractionation between hydrous Mg carbonates and aqueous solution observed in the laboratory is in close agreement with that found in the Salda Lake ecosystem (see Fig. 10). As Salda Lake is a closed basin, assuming the Mg concentration of the lake water is at steady state, the mass of Mg arriving to the lake must equal that precipitated in the form of Mg carbonates. Consequently, mass balance requires that the Mg isotopic offset between the naturally precipitated hydromagnesite and the Lake water is equal to that between the incoming streams and groundwaters and the Salda Lake water. This is consistent with observations reported above. A d26Mg offset of 0.9–1.6 % was measured between the Salda Lake water and the incoming streams and groundwaters; both naturally forming and laboratory synthesized hydrous Mg carbonates are isotopically 0.9–1.1 % lighter compared to their corresponding fluid phase. Furthermore, the difference in the lake water d26Mg composition between samples obtained during winter and summer periods may be attributed to increased carbonate mineral precipitation during the summer. It is important to note that the presence of biofilms and other heterotrophic bacteria reported in Salda Lake stromatolites (cf. Shcherbakova et al. 2010) apparently has an insignificant effect on the overall isotopic fractionation factor compared to the laboratory cyanobacteria monocultures. These observations support strongly the application of Mg isotopes to trace hydrous Mg carbonate precipitation in natural systems. It should nevertheless be pointed out that Mg isotope fractionation in natural systems may not be diagnostic of the biotic origin of precipitated hydrous Mg carbonates. Mavromatis et al. (2012a) reported that the Mg isotope fractionation found in abiotic precipitation experiments was nearly identical to that found in bacteria-present, nutrient-present experiments. This fractionation is also similar to that found in Salda Lake in the present study. These similarities refute the use of Mg isotopes to validate microbially mediated precipitation of hydrous Mg carbonates. Cyanobacteria photosynthesis is necessary to induce hydrous Mg carbonate precipitation, both for (1) increasing solution pH and fluid saturation state and (2) potentially to provide nucleation sites for aqueous carbonate.

0 10 20

Depth (m)

Fig. 10 Mg isotope composition in Salda Lake waters as a function of depth (blue diamonds), inflowing springs (pink rectangle), and hydromagnesite stromatolites and sediments (yellow rectangle)

30 40 Lake water

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Mineral/aqueous solution Mg isotope fractionation does not depend, however, on bacterial photosynthetic activity. Instead, this fractionation appears due exclusively to the stability of the distinct Mg isotopes in the mineral versus the fluid phase.

5 Conclusions This study provided the following insights in the processes of Mg isotope fractionation: 1. Both field and laboratory observations suggest that the presence of cyanobacteria promote Mg carbonate precipitation by increasing fluid pH (thus the fluid supersaturation state) and potentially by providing nucleation sites at the cell surface for mineral growth. As abiotic and nutrient-free experiments yielded no hydrous Mg carbonate precipitation, it can be concluded that the presence of photosynthesizing cyanobacterial cells is essential to the precipitation process. 2. A linear 1:1 molar dependence was observed between the amounts of Mg carbonate precipitated and bacterial biomass production. This observation is consistent with theoretical ratio of mineral precipitation during photosynthesis. This relationship may provide the means to reconstruct paleoproductivity based on the amount of accumulated Mg carbonate minerals. 3. Aqueous solution/mineral Mg isotope fractionation observed in the presence of Synechococcus sp. cyanobacteria in Salda Lake is identical to that found in laboratory experiments. Moreover, mass balance calculations performed on the Salda Lake system show a close match between Salda Lake water-hydromagensite fractionation and the Mg isotope offset between incoming rivers and the Salda Lake water. This coherence indicates that Mg isotopes may be a useful tool for tracing Mg carbonate precipitation. Nevertheless, as Mg fractionation in the biotic system is apparently identical to that in the abiotic system, the Mg isotopic signature of hydrous Mg carbonates cannot be used as a paleoproxy tool for validating microbial activity. Acknowledgments Jerome Chmeleff and Carole Causserand are acknowledged for their assistance with the MC-ICP-MS and atomic absorption analyses in Toulouse. This work was supported by ANR CO2-FIX, MC ITN DELTA-MIN (ITN-2008-215360), MC RTN GRASP-CO2 (MRTN-CT-2006-035868), and MC MIN-GRO (MRTN-CT-2006-035488) and the Associated European Laboratory LEAGE.

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