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Sulfate Reducing Bacteria: mechanisms of biomineralization and preservation of biosignatures of a key metabolism of Earth history – SRB

Biomineralization and preservation of biosignatures in the fossil record

Microbial metabolisms such as bacterial sulfate reduction are involved in the formation of key minerals widespread in the rock record, and might have played a central role in the coupling of S, C and Fe biogeochemical cycles in Earth history. Elucidating their role in ancient environments requires the use of robust biosignatures of these metabolisms. We explore these mechanisms of biomineralization using interdisciplinary tools, with the aim of defining / refining such biosignatures.

Experimental approach of microbial Fe biomineralization

Mineralogical diversity mirrors physiochemical variations at the Earth surface over geological timescales. Understanding how minerals form and in particular the role played by microorganisms, and attesting of their potential biogenecity requires clues to identify biosignatures recorded within minerals. This is all the more challenging than minerals are transformed upon diagenesis and metamorphism, which may erase or modify such biosignatures. <br />Sulfides are a good example of minerals that are ubiquitous in the geological record and witness the Earth surface redox conditions, such as the Gobal Oxygenation Event (2.5-2.0 Ga). Such minerals are also widely observed in exceptionally preserved fossils. <br />Although microbial sulfate reduction is usually invoked as a potential actor of sulfide biomineralization at low temperature, precise mechanisms controlling sulfide biomineralisation remain poorly constrained. For instance, extracellular organic polymers produced by microbes may play a role in the nucleation of these minerals. But metabolic activity surely plays a central role too. The parameters controlling this biomineralization remains thus to be explored, in particular down to the nm scale. <br />Eventually, given the strong connection between the activity of sulfate reducing bacteria and other metabolisms involved in Fe cycling in the environment, the coupling between these various metabolisms and their impact on the nature and properties of biomineralizatoin products remains to be evaluated.

Contributing to the identification of potential biosignatures of a metabolism requires an integrated, necessarily interdisciplinary, approach. This is why this project gathers geomicrobiologists, molecular biologists, isotope geochemists, electrochemists.
Moreover, exploring the mechanisms of biomineralization down to the nanometer scale is crucial to evidence potential local (chemical and structural) heterogeneities produced upon microbial activity.
We combine the study of natural samples (e.g. from lake Pavin) and biomineralization experiment using pure strains cultured under controlled conditions in the lab. Biomineralization products are characterized using a diversity of methods (electron microscopies, STXM, X-ray absorption spectroscopy).
Isotopic composition of biomineralization products will be explored as well (Fe, S), in order to define potential isotopic biosignatures as a function of culture conditions and mineral nature.
In addition, we combine biomineralization experiments and electrochemical methods in order to characterize and quantify the impact of microbial activity on the properties, composition and texture of biominerals. These methods are developed in collaboration with the LRCS (D. Larcher, N. Recham, Amiens), the Collège de France (J. M. Tarascon), the LCMCP (Christel Laberty-Robert) and the RS2E.
We also conduct experiments of experimental fossilisation of biominerals (S. Bernard, IMPMC) in order to model the evolution of organic matter and microbial biosignatures upon diagenetic conditions.

We studied two ferruginous lakes sharing some analogies with precambrian environments.
Lake Pavin is a meromictic lake (i.e. existence of a deep permanently anoxic layer), rich in iron and neutral pH. We characterized the mineralogical diversity with depth, as well as the geochemical properties of the lake in collaboration with the LGE (IPGP, D. Jézéquel). Our results show that numerous minerals exhibit typical textures and compositions of biominerals and suggest a tight coupling between microbial diversity and the mineralogy of at least one part of the solid phases formed in the water column (Miot et al. 2016, Minerals).
We studied a second lake (Lake 77), that is ferruginous and acidic, in collaboration with K. Küsel (Aquatic Geomicrobiology Lab, Univ. Jena). We characterized finely the evolution of Fe mineralogy with depth. We evidenced the mechanisms involved in the transformation / stabilisation of schwertmannite (Fe(III) hydroxysulfate, of microbial origin), as a function of the chemical conditions in the water column of the lake. These results suggest the combined role of chemical and microbiological processes governing mineral transformation/stabilization (e.g. pH variations, organic matter adsorption).

Future prospect includes:
* Culture of sulfate reducing bacteria under controlled conditions and biomineralization of Fe sulfides.
* Mineralogical and isotopic analyses.
* Combining biomineralization and electrochemistry.

Publications in peer-reviewed journals:
1. Miot J., Jézéquel D., Benzerara K., Cordier L., Rivas-Lamelo S., Skouri-Panet F., Férard C., Poinsot M., Duprat E. (2016) Mineralogical Diversity in Lake Pavin : connections with water column chemistry and biomineralization processes. Minerals, 6, 24.
2. J. Miot, Lu S., Morin G., Adra A., Benzerara K., Küsel K. (2016) Iron mineralogy across the oxycline of a lignite mine lake. Chemical Geology, doi : 10.1016/j.chemgeo.2016.04.013
3. Kish A., Miot J., Lombard C., Guigner J.M., S. Bernard, S. Zirah, Guyot F. (2016) Preservation of archeal surface layer structure during mineralization. Scientific Reports, in press.

1. Mirvaux B., Recham N., Tarascon J.M., Miot J. et al. (2015) Bacteria-assisted synthesis of Fe-based electrode materials for Li batteries. SFC 2015, Lille.
2. Miot J., Mirvaux B., Larcher D. et al. Biomineralization routes for the synthesis of Li-ion battery electrode materials. Colloque « Recherches inspirées de la Biodiversité », Paris, 2015.

Sulfate reducing bacteria (SRB) might have played a central role in Earth history, as they are involved in the biomineralization of sulfide minerals and in fine in the coupling of S, C and Fe biogeochemical cycles. They are also commonly thought to play a key role in the fossilization of soft tissues, by mediating their pyritization, sometimes leading to exceptional preservations in the fossil record. However, the biogenicity of sulfides found in the geologic record has been deeply controversed, the main reason being our poor understanding of the mechanisms of biomineralization of these mineral phases. Usual criteria of biogenicity rely on morphologial features as well as on isotopic signatures (S and Fe). Yet, such criteria suffer from an under-evaluation of the mechanisms controlling sulfide formation in the presence of SRB. Little is known regarding the role of organic phases involved in the nucleation of sulfides, the chemical parameters controlling sulfide formation, the potential of preservation of biosignatures under diagenetic conditions, ... Experimental models of microbial sulfate reduction and sulfide biomineralization would deeply extend our understanding of these mechanisms and allow us to define reliable biosignatures of this metabolism to be looked for in the fossil record.
The present project thus aims at elucidating the mechanisms of sulfide biomineralization by SRB, at determining biosignatures of this metabolism and at linking them to paleoenvironmental conditions, using an experimental approach. Different experimental systems will be designed in the laboratory: (i) the culture of diverse microbial strains isolated from modern environments, in particular from the « Precambrian analogue » lake Pavin (France) ; (ii) the co-culture of SRB and Fe-cycling bacteria in order to get insights into the coupling of Fe and S biogeochemical cycles and its consequences for the biomineralization of iron sulfides; (iii) the growth of electroactive (including SRB) biofilms at the surface of electrodes in microbial fuel cells, which will enable us to quantify electron transfers associated with metabolic and biomineralization activities. Based on these experimental systems, we propose to define new biosignatures of microbial sulfate reduction down to the nm-scale, based on (ultra-)structural, textural, chemical and electrochemical properties of the mineral-organic assemblages produced in our experimental systems. One of the breakthroughs of the present project will be to link bulk quantification of electron transfers associated with microbial redox activity to nm-scale redox heterogeneities left in minerals produced by these bacteria. In addition, isotopic fractionations of Fe and S will be calculated depending on the culture conditions, based on a detailed follow up of chemistry and mineralogy in these systems. This will provide us with new isotopic biosignatures of this metabolism. Finally, experimentally fossilized mineral-organic assemblages obtained in the laboratory will be characterized down to the nm-scale in order to evaluate the fate of the above-cited biosignatures upon diagenetic conditions. For this highly interdisciplinary project, we propose to gather experts in geomicrobiology, molecular biology, isotopy and electrochemistry. This interdisciplinarity is expected to persist beyond the timeframe of this proposal. In the end, this project will provide us with a solid understanding of sulfide biomineralization processes as well as with new biosignatures of this metabolism to be looked for in the fossil record.

Project coordination

Jennyfer Miot (Institut de Minéralogie, Physique des Matériaux et Cosmochimie)

The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.


IMPMC Institut de Minéralogie, Physique des Matériaux et Cosmochimie

Help of the ANR 250,151 euros
Beginning and duration of the scientific project: September 2014 - 48 Months

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