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Contrasting Taxonomic Stratification of Microbial Communities in Two Hypersaline Meromictic Lakes

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Contrasting Taxonomic Stratification of Microbial Communities in Two Hypersaline Meromictic Lakes The ISME Journal (2015) 9, 2642–2656 © 2015 International Society for Microbial Ecology All rights reserved 1751-7362/15 www.nature.com/ismej ORIGINAL ARTICLE Contrasting taxonomic stratification of microbial communities in two hypersaline meromictic lakes Adrian-Ştefan Andrei1,2,11, Michael S Robeson II3,4,11, Andreea Baricz2,5, Cristian Coman2,5, Vasile Muntean2, Artur Ionescu6, Giuseppe Etiope6,7, Mircea Alexe8, Cosmin Ionel Sicora9, Mircea Podar3,10 and Horia Leonard Banciu1,2 1Institute for Interdisciplinary Research in Bio-Nano-Sciences, Molecular Biology Center, Babeş-Bolyai University, Cluj-Napoca, Romania; 2Department of Molecular Biology and Biotechnology, Babeş-Bolyai University, Cluj-Napoca, Romania; 3Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, USA; 4Fish, Wildlife and Conservation Biology, Colorado State University, Fort Collins, CO, USA; 5National Institute of Research and Development for Biological Sciences (NIRDBS), Institute of Biological Research, Cluj-Napoca, Romania; 6Faculty of Environmental Science and Engineering, Babeş-Bolyai University, Cluj-Napoca, Romania; 7Istituto Nazionale di Geofisica e Vulcanologia, Rome, Italy; 8Faculty of Geography, Babeş-Bolyai University, Cluj-Napoca, Romania; 9Biological Research Center, Jibou, Romania and 10Department of Microbiology, University of Tennessee, Knoxville, TN, USA Hypersaline meromictic lakes are extreme environments in which water stratification is associated with powerful physicochemical gradients and high salt concentrations. Furthermore, their physical stability coupled with vertical water column partitioning makes them important research model systems in microbial niche differentiation and biogeochemical cycling. Here, we compare the prokaryotic assemblages from Ursu and Fara Fund hypersaline meromictic lakes (Transylvanian Basin, Romania) in relation to their limnological factors and infer their role in elemental cycling by matching taxa to known taxon-specific biogeochemical functions. To assess the composition and structure of prokaryotic communities and the environmental factors that structure them, deep- coverage small subunit (SSU) ribosomal RNA (rDNA) amplicon sequencing, community domain- specific quantitative PCR and physicochemical analyses were performed on samples collected along depth profiles. The analyses showed that the lakes harbored multiple and diverse prokaryotic communities whose distribution mirrored the water stratification patterns. Ursu Lake was found to be dominated by Bacteria and to have a greater prokaryotic diversity than Fara Fund Lake that harbored an increased cell density and was populated mostly by Archaea within oxic strata. In spite of their contrasting diversity, the microbial populations indigenous to each lake pointed to similar physiological functions within carbon degradation and sulfate reduction. Furthermore, the taxonomy results coupled with methane detection and its stable C isotope composition indicated the presence of a yet-undescribed methanogenic group in the lakes’ hypersaline monimolimnion. In addition, ultrasmall uncultivated archaeal lineages were detected in the chemocline of Fara Fund Lake, where the recently proposed Nanohaloarchaeota phylum was found to thrive. The ISME Journal (2015) 9, 2642–2656; doi:10.1038/ismej.2015.60; published online 1 May 2015 Introduction boundary layer (chemocline) (Boehrer and Schultze, 2009). These lakes are important model Meromictic (permanently stratified) lakes are dis- systems for aquatic biology research, because their tinct hydrological environments characterized by a constant vertical stratification, steep chemical persistent physicochemical stratification that cir- gradients and the presence of oxygen-deprived cumvents deep water recirculation. As a conse- zones favor niche partitioning among prokaryotic quence, they commonly comprise an upper stratum populations, enabling the study of vertical zonations where mixing occurs (mixolimnion), a stagnant in microbially-mediated biogeochemical cycling lower one (monimolimnion) and an interposing (Lauro et al., 2011; Lopes et al., 2011; La Cono et al., 2013). Correspondence: HL Banciu, Department of Molecular Biology Ursu and Fara Fund Lakes are 2 of the 41 and Biotechnology, Babeş-Bolyai University, 5-7 Clinicilor Street, permanent saline water bodies occurring in the Cluj-Napoca 400006, Romania. Transylvanian Basin (Romania) that were formed E-mail: [email protected] 11These two authors contributed equally to this work. between the eighteenth and nineteenth centuries Received 21 September 2014; revised 14 February 2015; accepted (Alexe, 2010) on the salt deposits produced by the 18 March 2015; published online 1 May 2015 Paratethys Sea evaporation (during the Badenian Prokaryotic diversity in hypersaline lakes A-S¸ Andrei et al 2643 salinity crisis, ca. 14 Myr ago). These two temperate The purpose of this study was to compare the lakes are unique among the other Romanian salt prokaryotic diversity and link it with limnological lakes because of their heliothermy (that is, trapping data in two distinct meromictic hypersaline lakes of solar radiation by a ‘saline lens’), size (that is, Ursu that differ in their hydric regimen, physicochemical Lake is one of the largest heliothermal salt lakes in characteristics, genesis and conservation status. Europe), conservation status (that is, Fara Fund Lake This would enable novel inferences regarding the is a protected area) and lake processes (that is, Ursu microbial ecology and geochemical cycles in bio- Lake is a natural lake whereas Fara Fund Lake is an energetically constrained stratified environments. To artificial one) (Alexe, 2010; Máthé et al., 2014). In achieve this aim, the vertical distribution and spite of their different genesis, they belong to the community structure of the prokaryotes thriving in same type of meromictic lakes, where the water the two lakes was investigated by combining deep- column overturn is hampered by strong salinity coverage small subunit (SSU) ribosomal RNA (rDNA) gradients. Although studies investigating the micro- amplicon sequencing, community domain-specific biota and substance turnover in meromictic lakes are quantitative PCR, chemical analyses and bioinfor- available (Biderre-Petit et al., 2011; Habicht et al., matics. Concentration and stable C isotope composi- 2011; Hamilton et al., 2014), most of the ones tion of dissolved methane and heavier alkanes were concerning the hypersaline water bodies were also analyzed for a preliminary assessment of performed on Arctic (Pouliot et al., 2009; Comeau microbial or other sources of hydrocarbons. et al., 2012) or Antarctic (Bowman et al., 2000; Lauro et al., 2011) lakes. Although information on tempe- rate neutral hypersaline meromictic lakes microbiota Materials and methods are scarce, previous investigations on Ursu Lake prokaryotes (using community-level physiological Site description and sampling profiling, culture-dependent and PCR–denaturing Ursu Lake (46°36’15 N; 25°05’09 E) is a natural gradient gel electrophoresis methods) have shown meromictic lake located at 505 m elevation in the the presence of active and diverse communities eastern part of the Transylvanian Basin. Having a (Cristea et al., 2014; Máthé et al., 2014); yet, a surface of 41 270 m2 and a maximum depth of 18.2 m detailed molecular diversity study is not available to (Figure 1b), it was formed in a depression caused by date. The microbial diversity of Fara Fund Lake has an intense process of salt dissolution between 1875 not been previously investigated, and hence the lake and 1880 (Alexe, 2010; Máthé et al., 2014). Cur- could constitute a valuable site for monitoring long- rently, it is exploited for recreational purposes term dynamics of microbial communities that are not during late-May to mid-August. Fara Fund under the impact of human activities. (45°52’34 N; 24°04’03 E) is an artificial meromictic Figure 1 Ursu Lake and Fara Fund Lake sampling sites. (a) Map showing the location of the lakes within Transylvanian Basin (Romania). The symbol size is not proportional with the sizes of the lakes. (b) Topo-bathymetric profile of Ursu and (c) Fara Fund lakes’ basins. The circles indicate the sampling points. The ISME Journal Prokaryotic diversity in hypersaline lakes A-S¸ Andrei et al 2644 pit lake situated at 383 m elevation in the southern combustion and infrared detection of CO2 released. area of the Transylvanian Basin (Figure 1a). Having a Both parameters (total nitrogen and total organic relatively small surface (∼1700 m2) and a maximum carbon) were measured according to EN 12260 and depth of 32 m (Figure 1b), this athalassic (sensu, EN 1484, respectively, using the multi N/C 2100S Hammer, 1986) lake was formed in 1775 on the area Analyzer (Analytik Jena, Jena, Germany). Relative of a late medieval bell-shaped salt mine that was shut expanded measurement uncertainty was calculated down at the end of the seventeenth century. according to International Organization for Standardi- Presently, it is declared as a protected area, as a zation—Guide to the expression of Uncertainty consequence of its strong heliothermy (Alexe, 2010). Measurement using a coverage factor (k)of2(k =2), The vertical sampling was carried out in October equivalent to a confidence of ∼ 95%. Uc ranged from 2013 using an inflatable boat positioned near the 4.5% to 13% depending on the compound as follows: 2+ − center of the lakes (Figures 1b and c). In situ 4.5% for Mg ;8%forHCO3, particulate Fe and 2+
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