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Groundwater Isolation Governs Chemistry and Microbial Community Structure Along Hydrologic Flowpaths

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Groundwater Isolation Governs Chemistry and Microbial Community Structure Along Hydrologic Flowpaths ORIGINAL RESEARCH published: 22 December 2015 doi: 10.3389/fmicb.2015.01457 Groundwater Isolation Governs Chemistry and Microbial Community Structure along Hydrologic Flowpaths Sarah Ben Maamar1,2,3 , Luc Aquilina2, Achim Quaiser1, Hélène Pauwels3, Sophie Michon-Coudouel4, Virginie Vergnaud-Ayraud2, Thierry Labasque2, Clément Roques2, Benjamin W. Abbott4 and Alexis Dufresne1* 1 OSUR-UMR 6553 ECOBIO, Université de Rennes 1 and Centre National de la Recherche Scientifique, Rennes, France, 2 OSUR-UMR 6118 Géosciences, Université de Rennes 1 and Centre National de la Recherche Scientifique, Rennes, France, 3 BRGM, Laboratory Department, Orléans, France, 4 OSUR-UMS 3343, Université de Rennes 1 and Centre National Edited by: de la Recherche Scientifique, Rennes, France Partha Basu, Duquesne University, USA Reviewed by: This study deals with the effects of hydrodynamic functioning of hard-rock aquifers on John W. Moreau, microbial communities. In hard-rock aquifers, the heterogeneous hydrologic circulation University of Melbourne, Australia strongly constrains groundwater residence time, hydrochemistry, and nutrient supply. Mustafa Yucel, Middle East Technical University, Here, residence time and a wide range of environmental factors were used to test Turkey the influence of groundwater circulation on active microbial community composition, Jarrod Scott, Bigelow Laboratory for Ocean assessed by high throughput sequencing of 16S rRNA. Groundwater of different Sciences, USA ages was sampled along hydrogeologic paths or loops, in three contrasting hard- *Correspondence: rock aquifers in Brittany (France). Microbial community composition was driven by Alexis Dufresne groundwater residence time and hydrogeologic loop position. In recent groundwater, in [email protected] the upper section of the aquifers or in their recharge zone, surface water inputs caused Specialty section: high nitrate concentration and the predominance of putative denitrifiers. Although This article was submitted to denitrification does not seem to fully decrease nitrate concentrations due to low Microbiological Chemistry and Geomicrobiology, dissolved organic carbon concentrations, nitrate input has a major effect on microbial a section of the journal communities. The occurrence of taxa possibly associated with the application of organic Frontiers in Microbiology fertilizers was also noticed. In ancient isolated groundwater, an ecosystem based on Received: 28 July 2015 Accepted: 04 December 2015 Fe(II)/Fe(III) and S/SO4 redox cycling was observed down to several 100 of meters Published: 22 December 2015 below the surface. In this depth section, microbial communities were dominated by Citation: iron oxidizing bacteria belonging to Gallionellaceae. The latter were associated to old Ben Maamar S, Aquilina L, Quaiser A, groundwater with high Fe concentrations mixed to a small but not null percentage of Pauwels H, Michon-Coudouel S, Vergnaud-Ayraud V, Labasque T, recent groundwater inducing oxygen concentrations below 2.5 mg/L. These two types Roques C, Abbott BW of microbial community were observed in the three sites, independently of site geology and Dufresne A (2015) Groundwater Isolation Governs Chemistry and aquifer geometry, indicating hydrogeologic circulation exercises a major control on and Microbial Community Structure microbial communities. along Hydrologic Flowpaths. Front. Microbiol. 6:1457. Keywords: aquifers, hydrology, 16S rRNA, pyrosequencing, groundwater, bacterial communities, iron oxidation, doi: 10.3389/fmicb.2015.01457 nitrate Frontiers in Microbiology | www.frontiersin.org 1 December 2015 | Volume 6 | Article 1457 Ben Maamar et al. Hydrology Governs Groundwater Chemistry and Diversity INTRODUCTION in the deeper fractured formation which is thus considered as partly isolated as compared to the surface layer which is actively Aquifers are populated by a vast diversity of microorganisms, recharged. some of which can play a critical role in subsurface Differences in hydrogeologic circulation and residence biogeochemical cycling and pollutant degradation (Yagi et al., time result in distinct groundwater geochemical composition, 2010). Because groundwater usually contains low concentrations e.g., modulating contributions of atmospheric oxygen and of organic carbon, microbial life there depends mostly on agricultural effluents. Annual recharge provides a relatively oxidation and reduction of inorganic compounds for energy. constant supply of oxygen from the surface to the weathered zone Thus, geochemical conditions, and in particular the availability of hard-rock aquifers, as well as chemical elements resulting from of electron donors and acceptors, are a major driver of microbial intensive agriculture such as nitrate and leaching of fertilizers. community composition and diversity in groundwater and the Conversely, groundwater in the fractured zone is relatively geological substratum (Akob et al., 2007; Boyd et al., 2007; Flynn protected and relatively isolated (Ayraud et al., 2008). However, et al., 2012, 2013; Nyyssönen et al., 2014). even regional hydrogeological loops are mixed to a certain degree Groundwater geochemistry is regulated in part by the to modern groundwater from the weathered zone and do not distribution of groundwater flow paths and groundwater represent fully isolated ecosystems. residencetime(Tarits et al., 2006; Roques et al., 2014a). To In this study, we assessed how groundwater partitioning date very few studies have addressed the effect of hydrology and isolation drives both groundwater hydrogeochemistry and on groundwater microbial communities, and those that have active microbial community structure in hard-rock aquifers by were restricted to a single aquifer (Roudnew et al., 2010; comparing surface recent groundwater considered as an opened Bougon et al., 2012; Larned, 2012; Lin et al., 2012; Zhou ecosystem, and old deep groundwater considered as partly et al., 2012). It is therefore imperative to assess the effects isolated, i.e., with low surface groundwater renewal. of groundwater circulation on microbial communities. The High-throughput sequencing based approaches such as 16S comparison of several aquifers with well-defined hydrogeologic rRNA gene profiling and metagenomics have made it possible conditions allows to constrain the influence of groundwater flow to explore complex groundwater microbial community and in order to better understand biogeochemical functioning of metabolism (Hemme et al., 2010; Lin et al., 2012; Smith groundwater ecosystems. et al., 2012; Wrighton et al., 2012; Castelle et al., 2013; Crystalline rocks represent about 35% of the continental Nyyssönen et al., 2014; Brown et al., 2015). Here, we collected surface (Blatt and Jones, 1975; Amiotte Suchet et al., 2003). groundwater samples from three geographically distinct aquifers They include crystalline aquifers also called hard-rock aquifers (Brittany, France, see Figure 1) where hydrogeologic and which constitute sensitive water resources that are increasingly hydrogeochemical parameters have been monitored for the last exploited (Foster and Chilton, 2003; Mall et al., 2006). Water 5 years allowing to determine residence times of groundwater. circulation in any aquifer is caused by the difference between We used pyrosequencing of 16S Ribosomal RNA amplicons the groundwater-table level in recharge zones high in the to characterize groundwater microbial communities, and to catchment, and the groundwater-table level in discharge zones infer putative microbial processes. As dissolved organic carbon in lowlands when the underground hydrogeologic catchment concentrations are below 1.3 mg/L in all the investigated sites is similar to the hydrologic surface catchment. That difference (Ayraud et al., 2006; Aquilina et al., 2015; Ploemeur monitoring induces a hydrogeologic gradient, generating hydrogeologic flow database http://hplus.ore.fr/), we hypothesized that heterotrophy paths or loops along the catchment slope (see Figure 1A for a remains limited at all depths. We also hypothesized that nitrate model of hydrogeologic circulations). More specifically, in hard- and oxygen are the major drivers in the weathered zone rock aquifers, the groundwater flow constitutes a topographic and that chemolithotrophic metabolisms linked to iron and flow system mainly in the near-surface weathered zone, which reduced sufur oxidation or sulfate reduction may occur in constitutes the upper layer of these aquifers (Wyns et al., 2004; the fractured zone which represents an interesting situation of Ayraud et al., 2008). Hydrogeologic loops may extend beneath very slow nutrient renewal, i.e., a transition state close to full the weathered layer into the fractured compartment where isolation. The investigation of three aquifers at the regional circulation takes place exclusively in networks of fractures (Wyns scale, with different hydrological conditions which are well et al., 2004; Ayraud et al., 2008). Large-scale regional loops constrained, allowed us investigating a more general case to may connect recharge and discharge zones over larger distances determine the relationships between microbial diversity and than the catchment size (i.e., hydrogeologic catchment is larger hydrology. than hydrologic catchment), causing inter-watershed exchanges and making it more difficult to define the recharge zone supplying large fracture discharges (Roques et al., 2014a; Aquilina MATERIALS AND METHODS et al., 2015). There is a partitioning between the weathered formation and the deeper fractured
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