Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids from the Laguna Negra Lake

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Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids from the Laguna Negra Lake Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids From the Laguna Negra Lake (Argentina) Estela Mlewski, Céline Pisapia, Fernando Gomez, Léna Lecourt, Eliana Soto Rueda, Karim Benzerara, Bénédicte Ménez, Stephan Borensztajn, Frédéric Jamme, Matthieu Refregiers, et al. To cite this version: Estela Mlewski, Céline Pisapia, Fernando Gomez, Léna Lecourt, Eliana Soto Rueda, et al.. Char- acterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids From the La- guna Negra Lake (Argentina). Frontiers in Microbiology, Frontiers Media, 2018, 9, pp.996 - 996. 10.3389/fmicb.2018.00996. hal-01824410 HAL Id: hal-01824410 https://hal.archives-ouvertes.fr/hal-01824410 Submitted on 27 Jun 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. ORIGINAL RESEARCH published: 22 May 2018 doi: 10.3389/fmicb.2018.00996 Characterization of Pustular Mats and Related Rivularia-Rich Laminations in Oncoids From the Laguna Negra Lake (Argentina) Estela C. Mlewski 1*†, Céline Pisapia 2,3†, Fernando Gomez 1, Lena Lecourt 2, Eliana Soto Rueda 1, Karim Benzerara 4, Bénédicte Ménez 2, Stephan Borensztajn 2, Frédéric Jamme 3, Matthieu Réfrégiers 3 and Emmanuelle Gérard 2* 1 Centro de Investigaciones en Ciencias de la Tierra (CICTERRA), Cordoba, Argentina, 2 Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Centre National de la Recherche Scientifique, Université Paris Diderot, Paris, France, 3 Synchrotron SOLEIL, DISCO Beamline, Saint Aubin, France, 4 Institut de Minéralogie, de Physique des Matériaux et de Edited by: Cosmochimie, UMR Centre National de la Recherche Scientifique 7590, Sorbonne Université, Muséum National d’Histoire Christophe Dupraz, Naturelle, IRD UMR 206, Paris, France Stockholm University, Sweden Reviewed by: Stromatolites are organo-sedimentary structures that represent some of the oldest Virginia Helena Albarracín, Center for Electron Microscopy records of the early biosphere on Earth. Cyanobacteria are considered as a main (CIME), Argentina component of the microbial mats that are supposed to produce stromatolite-like John Senko, structures. Understanding the role of cyanobacteria and associated microorganisms University of Akron, United States on the mineralization processes is critical to better understand what can be preserved *Correspondence: Estela C. Mlewski in the laminated structure of stromatolites. Laguna Negra (Catamarca, Argentina), a [email protected] high-altitude hypersaline lake where stromatolites are currently formed, is considered Emmanuelle Gérard [email protected] as an analog environment of early Earth. This study aimed at characterizing carbonate precipitation within microbial mats and associated oncoids in Laguna Negra. In particular, †These authors have contributed equally to this work. we focused on carbonated black pustular mats. By combining Confocal Laser Scanning Microscopy, Scanning Electron Microscopy, Laser Microdissection and Whole Genome Specialty section: Amplification, Cloning and Sanger sequencing, and Focused Ion Beam milling for This article was submitted to Transmission Electron Microscopy, we showed that carbonate precipitation did not Aquatic Microbiology, a section of the journal directly initiate on the sheaths of cyanobacterial Rivularia, which dominate in the mat. Frontiers in Microbiology It occurred via organo-mineralization processes within a large EPS matrix excreted Received: 30 January 2018 by the diverse microbial consortium associated with Rivularia where diatoms and Accepted: 27 April 2018 Published: 22 May 2018 anoxygenic phototrophic bacteria were particularly abundant. By structuring a large Citation: microbial consortium, Rivularia should then favor the formation of organic-rich laminations Mlewski EC, Pisapia C, Gomez F, of carbonates that can be preserved in stromatolites. By using Fourier Transform Infrared Lecourt L, Soto Rueda E, spectroscopy and Synchrotron-based deep UV fluorescence imaging, we compared Benzerara K, Ménez B, Borensztajn S, Jamme F, Réfrégiers M and Gérard E laminations rich in structures resembling Rivularia to putatively chemically-precipitated (2018) Characterization of Pustular laminations in oncoids associated with the mats. We showed that they presented a Mats and Related Rivularia-Rich Laminations in Oncoids From the different mineralogy jointly with a higher content in organic remnants, hence providing Laguna Negra Lake (Argentina). some criteria of biogenicity to be searched for in the fossil record. Front. Microbiol. 9:996. doi: 10.3389/fmicb.2018.00996 Keywords: Rivularia, carbonate precipitation, oncoids, Andean lakes, pustular mats Frontiers in Microbiology | www.frontiersin.org 1 May 2018 | Volume 9 | Article 996 Mlewski et al. Rivularia-Rich Lamination Related to Pustular Andean-Microbialites INTRODUCTION The Laguna Negra is a high-altitude hypersaline lake in Catamarca, Argentina where extreme environmental conditions Microbialites record microbial activities and (i.e., high UV-radiation and extreme temperature, salinity, sedimentary processes under a lithified form (Walter et al., and water activity) restrict eukaryotic life. Lithification is 1972; Burne and Moore, 1987). Stromatolites are laminated controlled by environmental processes (Gomez et al., 2014) microbialites probably produced by lithification of microbial along with microbial mats where diatoms and anoxygenic mats (Knoll, 2003; Bosak et al., 2007). Yet, comparable phototrophic bacteria are abundant (Gomez et al., 2018). This stromatolite-like products can form abiotically, casting doubts latter work focused on the texture, mineralogy and stable isotope on the biological origin of some fossil stromatolites (Buick geochemistry of subfossil oncoids and related microbialites from et al., 1981; Grotzinger and Knoll, 1999). Stromatolites are the Laguna Negra stromatolite belt. This belt mostly consists of pervasive in the Precambrian fossil record. They can be traced carbonated laminar crusts, stromatolites and oncoids. Different back to the early Archean, 3.43 billion years (Awramik and types of carbonate laminations were identified within the oncoids Sprinkle, 1999; Allwood et al., 2006) and even 3.7 billion years based on their texture (e.g., micritic, sparry, botryoidal, tufted ago (Nutman et al., 2016). Understanding the mechanisms of filament-rich palisade fabrics). These different laminations were stromatolite formation is thus mandatory for the quest of the partly associated with different microbial communities (i.e., oldest traces of life on Earth and for documenting the early Earth stratified pink colored, greenish and black pustular mats; Gomez environment. Notably, it is important to decipher the role played et al., 2018). Interestingly, laminations with calcified Rivularia- by microbial activity on the lithification processes. Microbial like cyanobacterial filaments showing tufted palisade fabrics metabolisms known to favor carbonate precipitation (by reaching were found alternating with micritic and botryoidal laminations. supersaturation with respect to carbonates through increased Consequently, potential changes in the microbial community alkalinity) include oxygenic and anoxygenic photosynthesis, could possibly be recorded within the oncoids as different types ureolysis, ammonification, denitrification, sulfate and iron of laminations. reduction, anaerobic sulfide oxidation, or methane oxidation The main objectives of this study were (i) to investigate (Dupraz and Visscher, 2005; Dupraz et al., 2009; Zhu and at Laguna Negra the potential role of a microbial consortium Dittrich, 2016). In addition, microbial exopolymeric substances forming the black pustular mat (BP) on the initiation of (EPS), consisting of a mixture of carbohydrates, proteins and carbonate precipitation and lamination formation and (ii) to nucleic acids, may promote or inhibit solid carbonate formation identify biogenicity criteria for the corresponding laminations (e.g., Benzerara et al., 2006), possibly depending on their in subfossil oncoids. By jointly using Confocal Laser Scanning divalent-cation binding capacity (Braissant et al., 2007; Glunk Microscopy (CLSM), Scanning and Transmission Electron et al., 2011). Among other phyla, cyanobacteria are important Microscopy (SEM/TEM) associated with Energy Dispersive X- producers of EPS in microbialites (e.g., Foster et al., 2009) ray Spectrometry (EDXS) and Focused Ion Beam (FIB) milling, and it has long been suggested that the formation of some as well as phylogenetic analyses on the bulk BP mat and on ancient stromatolites was mediated by oxygenic photosynthesis laser microdissected mat cells, we highlighted the presence of performed by cyanobacteria (Arp et al., 2001; Aloisi et al., an interesting microbial consortium associated with Rivularia 2006; Altermann et al., 2006; Riding, 2006). However, several filaments that triggers carbonate precipitation in the BP mats. studies have indicated that primary production in stromatolites In parallel, we determined the composition of the corresponding could be partly
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