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Prokaryotic and Eukaryotic Community Prokaryotic and Eukaryotic Community Structure in Field and Cultured Microbialites from the Alkaline Lake Alchichica (Mexico) Estelle Couradeau, Karim Benzerara, David Moreira, Emmanuelle Gerard, Jozef Kazmierczak, Rosaluz Tavera, Purificacion Lopez-Garcıa To cite this version: Estelle Couradeau, Karim Benzerara, David Moreira, Emmanuelle Gerard, Jozef Kazmierczak, et al.. Prokaryotic and Eukaryotic Community Structure in Field and Cultured Microbialites from the Alkaline Lake Alchichica (Mexico). PLoS ONE, Public Library of Science, 2012, 6 (12), pp.e28767. 10.1371/journal.pone.0028767. hal-00677228 HAL Id: hal-00677228 https://hal.archives-ouvertes.fr/hal-00677228 Submitted on 6 Aug 2020 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. Prokaryotic and Eukaryotic Community Structure in Field and Cultured Microbialites from the Alkaline Lake Alchichica (Mexico) Estelle Couradeau1,2,3, Karim Benzerara2, David Moreira1, Emmanuelle Ge´rard3,Jo´ zef Kaz´mierczak4, Rosaluz Tavera5, Purificacio´ nLo´ pez-Garcı´a1* 1 Unite´ d’Ecologie, Syste´matique et Evolution, CNRS UMR 8079, Universite´ Paris-Sud, Orsay, France, 2 Institut de Mine´ralogie et de Physique des Milieux Condense´s, CNRS UMR 7590, Universite´ Pierre et Marie Curie, Paris, France, 3 Institut de Physique du Globe de Paris, CNRS UMR 7154, Universite´ Paris Diderot, Paris, France, 4 Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland, 5 Departamento de Ecologı´a y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Auto´noma de Me´xico, Distrito Federal, Mexico Abstract The geomicrobiology of crater lake microbialites remains largely unknown despite their evolutionary interest due to their resemblance to some Archaean analogs in the dominance of in situ carbonate precipitation over accretion. Here, we studied the diversity of archaea, bacteria and protists in microbialites of the alkaline Lake Alchichica from both field samples collected along a depth gradient (0–14 m depth) and long-term-maintained laboratory aquaria. Using small subunit (SSU) rRNA gene libraries and fingerprinting methods, we detected a wide diversity of bacteria and protists contrasting with a minor fraction of archaea. Oxygenic photosynthesizers were dominated by cyanobacteria, green algae and diatoms. Cyanobacterial diversity varied with depth, Oscillatoriales dominating shallow and intermediate microbialites and Pleurocapsales the deepest samples. The early-branching Gloeobacterales represented significant proportions in aquaria microbialites. Anoxygenic photosynthesizers were also diverse, comprising members of Alphaproteobacteria and Chloroflexi. Although photosynthetic microorganisms dominated in biomass, heterotrophic lineages were more diverse. We detected members of up to 21 bacterial phyla or candidate divisions, including lineages possibly involved in microbialite formation, such as sulfate-reducing Deltaproteobacteria but also Firmicutes and very diverse taxa likely able to degrade complex polymeric substances, such as Planctomycetales, Bacteroidetes and Verrucomicrobia. Heterotrophic eukaryotes were dominated by Fungi (including members of the basal Rozellida or Cryptomycota), Choanoflagellida, Nucleariida, Amoebozoa, Alveolata and Stramenopiles. The diversity and relative abundance of many eukaryotic lineages suggest an unforeseen role for protists in microbialite ecology. Many lineages from lake microbialites were successfully maintained in aquaria. Interestingly, the diversity detected in aquarium microbialites was higher than in field samples, possibly due to more stable and favorable laboratory conditions. The maintenance of highly diverse natural microbialites in laboratory aquaria holds promise to study the role of different metabolisms in the formation of these structures under controlled conditions. Citation: Couradeau E, Benzerara K, Moreira D, Ge´rard E, Kaz´mierczak J, et al. (2011) Prokaryotic and Eukaryotic Community Structure in Field and Cultured Microbialites from the Alkaline Lake Alchichica (Mexico). PLoS ONE 6(12): e28767. doi:10.1371/journal.pone.0028767 Editor: Jack Anthony Gilbert, Argonne National Laboratory, United States of America Received September 13, 2011; Accepted November 14, 2011; Published December 14, 2011 Copyright: ß 2011 Couradeau et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This project was financed by the French Centre National de la Recherche Scientifique - CNRS Interdisciplinary program ‘‘Origines des plane`tes et de la vie’’ (PID OPV) and Institut National des Sciences de l’Univers - INSU program ‘‘InteractionsTerre/Vie’’ (InterrVie), and the Polish Ministry of Science and Higher Education grant N307019. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Purificacion Lopez-Garcia is an Academic Editor of PLoS ONE. This does not alter the authors’ adherence to all the PLoS ONE policies on sharing data and materials. * E-mail: [email protected] Introduction Turkey [12,13], Pyramid Lake, USA [14], the Indonesian crater lakes Satonda [15,16,17] and Niuafo’ou [18], but also in the Microbialites are organosedimentary structures formed by freshwater Ruidera pools [19] and the hypersaline lakes microbially-mediated mineral precipitation and/or accretion [1]. LagoVermelha, Brazil [20] and Cuatro Cie´nagas, Mexico [21]. Stromatolites are microbialites exhibiting a laminated macrofabric Despite their geological and evolutionary importance, the precise [2]. Their fossils are found throughout the geological record [3,4], stromatolite formation mechanisms remain poorly understood. It the oldest being 3,43 Ga old (Pilbara Craton, Western Australia) has been proposed that net carbonate precipitation results from a [5]. After having dominated the Precambrian, stromatolite balance between concurrent microbial metabolisms [22]. Photo- abundance declined steeply at the onset of the Phanerozoic synthesis (both oxygenic and anoxygenic) and sulfate reduction lead [6,7]. Today, stromatolites are confined to very few marine or to local carbonate supersaturation, whereas heterotrophic metab- quasi-marine environments, such as the well-studied Shark Bay, olisms induce carbonate dissolution [23,24,25,26]. In addition, Australia [8,9] and Exuma Sound, Bahamas [10,11]. Microbialites massive cyanobacterial production of exopolymeric substances have also been described in alkaline lakes such as Lake Van, (EPS), which efficiently sequester cations such as Ca2+ or Mg2+, PLoS ONE | www.plosone.org 1 December 2011 | Volume 6 | Issue 12 | e28767 Alchichica Crater Lake Microbialite Communities can also inhibit carbonate precipitation [27]. Hence, microbialite Table 1. Alchichica samples analyzed in this study. formation most likely results from the interplay between microor- ganisms forming complex communities and their metabolic activities under the influence of environmental conditions (e.g. Sample Origin Description photoperiod, temperature) and local chemistry (ion availability). The characterization of microbial diversity is thus crucial to AL29 0,08 m microbialite fragment, black/dark brown further understand microbe-mineral interactions in microbialites. AL31* 0,5 m microbialite fragment, black/dark brown Most diversity studies using molecular methods have focused on AL27 0,8 m microbialite fragment, black/dark brown marine stromatolites, where Alpha- and Gammaproteobacteria, AL43 1 m microbialite fragment, dark brown Cyanobacteria and Planctomycetales appear to dominate AL36 1,5 m microbialite fragment, dark brown [28,29,30,31,32,33,34,35]. In contrast, knowledge about lacustrine microbialites remains much sparser. Firmicutes, Gamma- and AL38 2 m microbialite fragment, dark brown Alphaproteobacteria were the most abundant taxa in Lake Van AL70 3 m microbialite fragment, brown microbialites, but these studies were carried out on 15 year-old dry AL67* 4 m microbialite fragment, brown/dark green samples and, hence, probably biased [13]. Recent metagenomic AL64 5 m microbialite fragment, dark green analysis of Cuatro Cie´nagas microbialites revealed a complex AL61 6 m microbialite fragment, green community where Cyanobacteria, Alpha- and Gammaproteobac- AL58 8 m microbialite fragment, intense emerald green teria and Planctomycetales predominated, as in marine micro- bialites, identifying functions potentially linked to complex redox- AL55 11 m microbialite fragment, intense green/yellowish dependent activities and the establishment of structured biofilms AL52* 14 m microbialite fragment, golden/brownish [21]. Despite these pioneering studies, the precise role in AQ1* Aquarium 1 microbialite fragment mineralization and biofilm dynamics of many bacterial taxa, but AQ1b Aquarium 1 aquarium glass wall biofilm also of the much less studied eukaryotic and archaeal
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