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Microbial Lithification in Marine Stromatolites and Hypersaline Mats

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Microbial Lithification in Marine Stromatolites and Hypersaline Mats View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library Published in Trends in Microbiology 13,9 : 429-438, 2005, 1 which should be used for any reference to this work Microbial lithification in marine stromatolites and hypersaline mats Christophe Dupraz1 and Pieter T. Visscher2 1Institut de Ge´ ologie, Universite´ de Neuchaˆ tel, Rue Emile-Argand 11, CP 2, CH-2007 Neuchaˆ tel, Switzerland 2Center for Integrative Geosciences, Department of Marine Sciences, University of Connecticut, 1080 Shennecossett Road, Groton, Connecticut, 06340, USA Lithification in microbial ecosystems occurs when pre- crucial role in regulating sedimentation and global bio- cipitation of minerals outweighs dissolution. Although geochemical cycles. the formation of various minerals can result from After the decline of stromatolites in the late Proterozoic microbial metabolism, carbonate precipitation is pos- (ca. 543 million years before present), microbially induced sibly the most important process that impacts global and/or controlled precipitation continued throughout the carbon cycling. Recent investigations have produced geological record as an active and essential player in most models for stromatolite formation in open marine aquatic ecosystems [9,10]. Although less abundant than in environments and lithification in shallow hypersaline the Precambrian, microbial precipitation is observed in a lakes, which could be highly relevant for interpreting the multitude of semi-confined (physically or chemically) to rock record and searching for extraterrestrial life. Two confined macro- and micro-environments, from the deep factors that are controlled by microbial processes and sea to shallow platforms and terrestrial deposits. physicochemical characteristics determine precipi- Microbial precipitation is proposed to have a role in the tation: exopolymeric substances and the saturation formation of sedimentary carbonate sedimentary particles index, the latter being determined by the pH, {Ca2C} [11,12], and terrestrial consortia of microorganisms 2K and {CO3 }. Here, we evaluate community metabolism through oxalate-carbonate transformation can sequester in microbial mats and hypothesize why these organo- large amounts of CO2 by precipitating CaCO3 [13,14]. sedimentary biofilms sometimes lithify and sometimes Lithifying microbial communities seem to be crucial to the do not. settlement and edification of reefs through stabilization of sediments and in filling the porosity inside the reef body through precipitation. In Mesozoic coral and sponge reefs, for example, microbially induced precipitation supported Lithification in the history of the Earth construction of a rigid framestone by ‘cementing’ the Approximately 3.5–3.8 billion years ago, at the onset of life macrofauna inside the reef [15,16]. Even in the absence of on our planet, complex microbial communities formed. macroscopic metazoans, microbes continue to build reef- These microbial communities orchestrated the precipi- like structures, such as mud mounds in the deeper oceans, tation of calcium carbonate and the formation of stroma- the ecological implications of which are still poorly understood [10,17]. tolites, recording a permanent imprint of their presence on Stromatolitic structures are among the earliest macro- the Earth [1,2]. Stromatolites are lithifying organosedi- scopic evidence for life on Earth [10,18], which raises the mentary structures formed by trapping and binding of question of how precipitation and dissolution of minerals sediment and/or the net carbonate-precipitating activities is facilitated by microorganisms. Microbially mediated of microorganisms, resulting in a layered structure. As the precipitation is not limited to carbonates but might also first photosynthetic communities, proliferating in the comprise other minerals, such as silicates and sulfates shallow zone of the oceans, they consumed the greenhouse (e.g. gypsum, anhydrite) [9]. Here, we explore calcium gas CO , and produced free O [3,4] and H [5]. The 2 2 2 carbonate precipitation and dissolution as a result of evolutionary processes that drove the formation of these coupled microbial metabolism (altering, for example the lithifying prokaryotic communities remain largely carbonate alkalinity and pH) and geochemical reactions. uncharacterized [6], although it has been speculated We focus on sedimentary biofilms in modern marine and that microbial lithification resulted as a by-product of hypersaline environments to potentially aid interpreta- metabolism [7] or as a direct consequence of microbes tion of the rock record and search for extraterrestrial life. harvesting energy from protons released during calcium carbonate (CaCO3) precipitation [8]. Regardless of origin, microbial lithification represents what could be seen as a Requirements for lithification major evolutionary advance that enabled stromatolites to There are several models for lithification, ranging from thrive for almost 85% of the Earth’s history [1], having a entirely microbial [19–22] to purely chemically mediated Corresponding author: Visscher, P.T. ([email protected]). mechanisms [23]. Cyanobacteria have been implicated in CaCO3 precipitation (for example, see Ref. [13]) (Figure 1), 2 GROUPS LIGHT DARK Cyanobacteria – 2+ 2HCO3 + Ca [CH2O] + CaCO3 + O2 0 Oxygen (µM) 1500 0 Oxygen (µM) 1500 Fermentation – N2 fixation 0 Sulfide (µM) 800 0 Sulfide (µM) 800 Aerobic heterotrophs O2 – 2+ [CH2O] + CaCO3 + O2 HCO3 + Ca O2 Fermentation – Denitrification Anoxygenic phototrophs – 2+ – 2– 3HCO3 + Ca + HS [CH2O] + CaCO3 + SO4 Ca2+ Ca2+ Fermentation – synthesis of Bchlα – Depth degradation of glycogen Depth pH pH Sulfate reducers 2– – 2+ 2[CH2O] + SO4 + OH + Ca – CaCO3 + CO2 + 2H2O + HS Sulfide oxidizers 3HS– + 4O + CaCO + HCO – 2 3 3 – – 2+ 2– HS HS 2[CH2O] + Ca + 3SO4 Fermentation – denitrification 6 pH 11 Fermenters (e.g. ethanol) 6 pH 11 0 Calcium (mM) 50 – 2+ 0 Calcium (mM) 50 3[CH2O] + CaCO3 + H2O HCO3 + Ca + C2H6O Coupled element cycling Photosynthesis Cell material CO2 Oxy-photosynthesis Anox-photosynthesis Inorganic C O Aer-respirS ationN Fe Organic C Anaer-respiration Metabolic (SI) Aer-fermentation Chemical control control on EPS on CaCO CaCO3 3 precipitation precipitation Respiration TRENDS in Microbiology Figure 1. Metabolic pathways and geochemical gradients in a lithifying microbial mat. Six major groups of microbes composing the microbial mat community impact calcium carbonate precipitation and dissolution through metabolic activities (as outlined in the coupled microbial–geochemical equations presented in the main text). Combined metabolic activities determine the net precipitation potential and also the vertical geochemical gradients (left and right panels). Note the extreme diel fluctuations of oxygen, sulfide and pH caused by dependence of photosynthesis on light. Differences in day and night metabolism (temporal separation; redrawn from actual measurements) and a certain degree of vertical structuring of the various metabolic reactions (spatial separation) cause local differences in the saturation index (SI), ultimately regulating chemical precipitation. The calcium profile shows a minimum due to sequestration by the exopolymeric substances (EPS), which is most abundant in the layer of maximum photosynthesis. Carbon cycling (bottom part of figure) is coupled to element cycles of O, S and N, as these provide electron donors for C-fixation and electron acceptors for respiration, respectively. Preferential use of a certain cycle over another yields a greater precipitation potential (e.g. SOO) [21,27,28]. Similarly, excess carbon fixation enables, for example, EPS build-up, whereas excess anaerobic respiration favors precipitation through an increased SI [28]. as have aerobic heterotrophs [12] and sulfate-reducing and (ii) a biological–chemical facet, exopolymeric sub- bacteria (SRB) [24–27]. Although precipitation has been stances (EPS). The saturation index is defined as SIZ well-studied and dissolution of carbonates has been largely log(IAP/Ksp), where IAP denotes the ion activity product 2C 2K neglected, it should be noted that net precipitation results (i.e. {Ca }!{CO3 }) and Ksp, the solubility product of the from the balance of these two processes [28]. Pinckney and corresponding mineral (10K6.19 and 10K6.37 for aragonite Reid [20] proposed a balance between photosynthesis (P) and calcite, respectively, at 258C, 1 bar atmospheric and respiration (R): if POR then precipitation would take pressure and 35 PSU salinity [29]). If IAPOKSP, then place; if P!R, dissolution would follow. the solution is supersaturated, and when SIO0.8, then 2K Two crucial factors that support CaCO3 precipitation CaCO3 precipitates [30]. The [CO3 ] depends on the K 2 emerge: (i) a geochemical facet, the saturation index (SI), carbonate equilibrium (H2CO3 4HCO3 4CO3 ; pKa of 5.9 3 INHIBITION OF PRECIPITATION Alveolar EPS matrix depending on Ca2+-binding capacity with carboxyl group Ca2+ 2+ R R Ca Production of EPS Adsorption of Ca2+ by cyanobacteria (and other cations) and other microbes ALTERATION OF EPS Reduction of cation-binding capacity (1) (2) (3) Enhancement of precipitation Microbial EPS degradation Organomineralization Saturation of binding capacity Carbonate layer Ca2+ Ca2+ Ca2+ Ca2+ R R R R Ca2+ Ca2+ Organic template Ca2+ 2+ Ca liberation Alteration of EPS yields HCO – CO 2– Satutation of the cation binding 3 3 reorganization of acidic capability, terminates inhibition sites in template that allows
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