Microbialite Genetic Diversity and Composition Relate to Environmental Variables Carla M
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RESEARCH ARTICLE Microbialite genetic diversity and composition relate to environmental variables Carla M. Centeno1, Pierre Legendre2, Yislem Beltra´ n1, Rocı´o J. Alca´ ntara-Herna´ ndez1, Ulrika E. Lidstro¨ m3, Matthew N. Ashby3 & Luisa I. Falco´ n1 1Instituto de Ecologı´a, Universidad Nacional Auto´ noma de Me´ xico, Mexico City, Mexico; 2De´ partement de Sciences Biologiques, Universite´ de Montre´ al, Montre´ al, QC, Canada; and 3Taxon Biosciences, Inc., Tiburon, CA, USA Correspondence: Luisa I. Falco´ n, Instituto de Abstract Ecologı´a, Universidad Nacional Auto´ noma de Me´ xico, 3er Circuito Exterior sn, Ciudad Microbialites have played an important role in the early history of life on Universitaria, Del. Coyoaca´ n, Mexico D.F. Earth. Their fossilized forms represent the oldest evidence of life on our planet 04510. Tel.: +52 55 5622 8222, ext. 46869; dating back to 3500 Ma. Extant microbialites have been suggested to be highly fax: 52 55 5622 8995; e-mail: productive and diverse communities with an evident role in the cycling of [email protected] major elements, and in contributing to carbonate precipitation. Although their ecological and evolutionary importance has been recognized, the study of their Received 30 March 2012; revised 28 June 2012; accepted 29 June 2012. genetic diversity is yet scanty. The main goal of this study was to analyse Final version published online 2 August 2012. microbial genetic diversity of microbialites living in different types of environ- ments throughout Mexico, including desert ponds, coastal lagoons and a DOI: 10.1111/j.1574-6941.2012.01447.x crater-lake. We followed a pyrosequencing approach of hypervariable regions of the 16S rRNA gene. Results showed that microbialite communities were very Editor: Gary King diverse (H′ = 6–7) and showed geographic variation in composition, as well as an environmental effect related to pH and conductivity, which together Keywords explained 33% of the genetic variation. All microbialites had similar propor- microbialites; microbial communities; tions of major bacterial and archaeal phyla. diversity; composition; pyrosequencing. (Allwood et al., 2006; Schopf et al., 2007). The micro- Introduction bial communities associated to these fabrics establish Microbialites are complex organo-sedimentary structures complex ecological associations that occur vertically, that trap, bind and precipitate detritus and minerals such stratified in visible millimeter scale layers (DesMarais, as carbonates, silicates and sulphates (Dupraz et al., 2009) 1995; Stal, 1995), forming small-scale ecosystems consti- through the activity of their biological constituents tuted by a variety of metabolically and phylogenetically (Burne & Moore, 1987; Paerl et al., 2001; Dupraz & distinct taxa (Burne & Moore, 1987; Paerl et al., 2001). Visscher, 2005; Desnues et al., 2008). Hence, their charac- Microbialites have been argued to be the first organized teristics and structural properties are the products of bio- ecosystems on the planet, where transformations of logical and ecological factors (Foster et al., 2009; Last major constitutive elements are coupled to microbial et al., 2010). They can show various degrees of lithifica- metabolism (van Gemerden, 1993; Decho et al., 2005; tion (Sprachta et al., 2001), differences in morphology, Leuko et al., 2007; Paterson et al., 2008). The actively mode of growth and substrate (Pringault et al., 2005). growing portion of microbialites, which occurs in the The grain size of the substrate, capillary attraction of surface layers, has been compared in terms of produc- À À water, penetration of light, sedimentation–erosion rates, tivity (5000–6200 mg cm 2 day 1) to tropical forests À À wave action, grazing pressure (van Gemerden, 1993), (6000 mg cm 2 day 1), where a vast contribution of inorganic and biologically mediated calcification (Burne phototrophs, both oxygenic and anoxygenic, has been & Moore, 1987) are fundamental for microbialite devel- recognized (Stal, 2000). Microbialites are also known MICROBIOLOGY ECOLOGY MICROBIOLOGY opment (Dupraz & Visscher, 2005). for their role in the N cycle harboring an important Extant microbialites are the nearest analogues to fos- diversity of N2-fixing phyla (Stal et al., 2010). silized stromatolites, which consist of the oldest evi- Despite the ecological and evolutionary relevance of dence of life on Earth, dating back to 3500 Ma microbialites, the study of their genetic composition is ª 2012 Federation of European Microbiological Societies FEMS Microbiol Ecol 82 (2012) 724–735 Published by Blackwell Publishing Ltd. All rights reserved Microbialite genetic diversity and composition 725 relatively recent (Burns et al., 2004; Papineau et al., 1994) where we sampled the Rio Mesquites (RM) perma- 2005; Mobberley et al., 2012). Historically, Cyanobacteria nent stream. have been the most studied phylum, and their relevance as phototrophs and diazotrophs in the formation of the Central Mexico microbial tapestry and morphogenesis of microbialites has been recognized (Reid et al., 2000; Neilan et al., This region is characterized by the Trans Mexican 2002; Dupraz & Visscher, 2005; Pringault et al., 2005; Volcanic Belt, including several crater-lakes. Alchichica Kromkamp et al., 2007; Foster et al., 2009; Gischler is the largest of these limnetic bodies and is a maars- et al., 2011). However, the identification of other bacte- alkaline and athalasohaline system with particular fea- rial and archaeal taxa associated to microbialites has tures including relatively high electric conductivity, remained limited (Breitbart et al., 2009; Burns et al., subsaline water, as well as high contents of magnesium 2009; Bolhuis & Stal, 2011; Mobberley et al., 2012). and calcium carbonates (Couradeau et al., 2011). Cabal- Although robust diversity estimations have been done lero et al. (2003) mentioned that the main factors using different molecular ecology techniques, to date no responsible for the chemistry of this lake are influx of single study had been conducted in which both geo- water rich in sodium from volcanic materials, and graphic and environmental gradients were included to bicarbonates from Cretaceous limestone. Previous work identify potential abiotic variables that contribute to by Tavera & Koma´rek (1996) described columnar and microbialite community composition. Microbialites are spongy microbialites in Alchichica, following a micros- known to occur in several environments throughout copy-based identification strategy. Recent studies by Ka- Mexico (Gischler et al., 2008, 2011; Breitbart et al., zmierczak et al. (2011) identified that both microbialite 2009; Kazmierczak et al., 2011; Beltra´n et al., 2012), a morphologies comprised two generations and had mega diverse country, in which species turnover differences in mineral composition, the spongy-types increases due to strong environmental gradients. The being composed mainly of hydromagnesite with an aim of this study was to analyse whether microbial com- admixture of huntite and calcite, and dating to approx- munity composition, described using a pyrosequencing imately 2800 years B.P., and the columnar-types being approach of hypervariable regions of the 16S rRNA composed of aragonite and an admixture of Mg-calcite, gene, had a structuring effect related to environmental dating to approximately 1100 years B.P. The different variables along a latitudinal gradient. morphologies of Alchichica’s microbialites are attributed to different environmental conditions, where the spongy forms would relate to a dry period and the columnar Materials and methods forms to a wet climate associated to large inflow of ground water. In this study we included both microbia- Site description and sampling lite morphotypes (columnar AC, and spongy AS). Microbialites were collected in the summer of 2009 from 10 localities distributed throughout Mexico (Fig. 1, Southern Mexico-Yucatan Peninsula Table 1). The Yucatan Peninsula is a carbonate platform that began to emerge above sea level during the Oligocene and Mio- cene (Ferrusquia-Villafranca, 1993). The entire peninsula Northern Mexico consists of karstic landscapes (Gischler et al., 2008, 2011). The Cuatro Cienegas Basin (CCB) consists of the largest In this study we sampled two coastal lagoons: Muyil, oasis in the Chihuahuan Desert, where microbialites are inside the Sian Ka‘an Biosphere Reserve, where we conspicuous features in some of the more than 200 ponds, included microbialites (SS) and a microbial mat (SM); lakes and streams. The region is characterized by steeply Laguna Bacalar, near the Mexico–Belize border, is the folded Cretaceous sediments (Johannesson et al., 2004), freshwater site with the largest occurrence of extant where ‘Sierra de San Marcos’ is a faulted anticline com- microbialites (Gischler et al., 2008, 2011). Sampling posed of cretaceous shallow water limestone, dolomite and included the Pirate Channel (BP), Los Rapidos (BR) and gypsum (Garcia-Pichel et al., 2004). Sampling sites a soft, low degree of induration formation (BM). Bacalar included the Pozas Azules Ponds (PI and PII) that are microbialites have been radiometrically dated between found along the ‘Sierra de San Marcos’, where the vertical 6790 and 9190 years B.P., corresponding to early Holo- canyon slopes are rimmed by Quaternary karstified alluvial cene (Gischler et al., 2008), making them the oldest fans, giving way to a flat desert floor (Winsborough et al., known extant microbialites. FEMS Microbiol Ecol 82 (2012) 724–735 ª 2012 Federation