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Increases in the Abundance of Microbial Genes Encoding Halotolerance and Photosynthesis Along a Sediment Salinity Gradient Tc Jeffries, Jr Seymour, K

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Increases in the Abundance of Microbial Genes Encoding Halotolerance and Photosynthesis Along a Sediment Salinity Gradient Tc Jeffries, Jr Seymour, K Increases in the abundance of microbial genes encoding halotolerance and photosynthesis along a sediment salinity gradient Tc Jeffries, Jr Seymour, K. Newton, Rj Smith, Laurent Seuront, J. Mitchell To cite this version: Tc Jeffries, Jr Seymour, K. Newton, Rj Smith, Laurent Seuront, et al.. Increases in the abundance of microbial genes encoding halotolerance and photosynthesis along a sediment salinity gradient. Biogeo- sciences, European Geosciences Union, 2012, 9, pp.815-825. 10.5194/bg-9-815-2012. hal-00815398 HAL Id: hal-00815398 https://hal.archives-ouvertes.fr/hal-00815398 Submitted on 12 Mar 2021 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. Distributed under a Creative Commons Attribution| 4.0 International License Biogeosciences, 9, 815–825, 2012 www.biogeosciences.net/9/815/2012/ Biogeosciences doi:10.5194/bg-9-815-2012 © Author(s) 2012. CC Attribution 3.0 License. Increases in the abundance of microbial genes encoding halotolerance and photosynthesis along a sediment salinity gradient T. C. Jeffries1,2, J. R. Seymour2, K. Newton1, R. J. Smith1, L. Seuront1,3,4, and J. G. Mitchell1 1School of Biological Sciences, Flinders University, Adelaide, South Australia 5001, Australia 2Plant Functional Biology and Climate Change Cluster, University of Technology Sydney, Australia 3Aquatic Sciences, South Australian Research and Development Institute, Henley Beach 5022, Australia 4Centre National de la Recherche Scientifique, Paris cedex 16, France Correspondence to: T. C. Jeffries ([email protected]) Received: 14 July 2011 – Published in Biogeosciences Discuss.: 28 July 2011 Revised: 30 January 2012 – Accepted: 31 January 2012 – Published: 20 February 2012 Abstract. Biogeochemical cycles are driven by the 1 Introduction metabolic activity of microbial communities, yet the envi- ronmental parameters that underpin shifts in the functional Biogeochemical cycles, over geological time, have funda- potential coded within microbial community genomes are mentally determined the chemical nature of the Earth’s sur- still poorly understood. Salinity is one of the primary de- face and atmosphere. Due to their high abundance and terminants of microbial community structure and can vary metabolic activities, microorganisms drive many global bio- strongly along gradients within a variety of habitats. To geochemical processes including the carbon, oxygen, nitro- test the hypothesis that shifts in salinity will also alter the gen, hydrogen, sulfur and iron cycles (Falkowski et al., 2008; bulk biogeochemical potential of aquatic microbial assem- Fuhrman, 2009). The biochemical potential of the micro- blages, we generated four metagenomic DNA sequence li- bial inhabitants of an environment is determined by the com- braries from sediment samples taken along a continuous, nat- munity structure – the types of organisms present and their ural salinity gradient in the Coorong lagoon, Australia, and relative abundance, which is in turn largely determined by compared them to physical and chemical parameters. A total the physico-chemical conditions of the habitat, such as the of 392483 DNA sequences obtained from four sediment sam- need for cells to survive in highly saline environments by ad- ples were generated and used to compare genomic character- justing their internal salt concentrations (Oren, 2009). How istics along the gradient. The most significant shifts along microbial communities respond to and contribute to chemi- the salinity gradient were in the genetic potential for halotol- cal gradients is a central question of microbial ecology and erance and photosynthesis, which were more highly repre- is essential to our understanding of biogeochemical cycling sented in hypersaline samples. At these sites, halotolerance and biological adaptation to global change. was achieved by an increase in genes responsible for the ac- Salinity has an important influence on the global distri- quisition of compatible solutes – organic chemicals which in- bution of bacterial diversity (Lozupone and Knight, 2007). fluence the carbon, nitrogen and methane cycles of sediment. Salinity gradients occur in a wide variety of ecologically im- Photosynthesis gene increases were coupled to an increase portant habitats such as estuaries, wetlands, salt marshes and in genes matching Cyanobacteria, which are responsible for coastal lagoons. Many of these habitats are under increasing mediating CO2 and nitrogen cycles. These salinity driven pressure from climate change, due to increased evaporation, shifts in gene abundance will influence nutrient cycles along reduced freshwater flows, and rising sea levels (Scavia et al., the gradient, controlling the ecology and biogeochemistry of 2002; Schallenburg et al., 2003). the entire ecosystem. In high salinity environments, microbes must maintain their cellular osmotic balance via the acquisition of charged solutes (Roberts, 2005; Oren, 2009). This fundamen- tal physiological requirement has led to the evolution of Published by Copernicus Publications on behalf of the European Geosciences Union. 816 T. C. Jeffries et al.: Increases in the abundance of microbial genes halotolerant specialists, with several studies in hypersaline ford et al., 2011). A better knowledge of the response of habitats demonstrating that microbial diversity decreases microbial communities to these conditions is essential from with salinity (Estrada et al., 2004; Schapira et al., 2010; the perspective of both (i) ecosystem management and (ii) Pedros-Ali´ o´ et al., 2000; Benlloch et al., 2002) with halo- as a model to understand the effect of increased salinity lev- tolerant and halophilic taxa becoming dominant in more ex- els on microbially mediated biogeochemical cycles. While treme salinities. Shifts in microbial community structure microbial and viral abundance and activity has been shown have also been observed along estuaries (Bouvier and del to increase along this salinity gradient (Schapira et al., 2009, Giorgio, 2002; Oakley et al., 2010; Bernhard et al., 2005) 2010; Pollet et al., 2010), the identity and metabolic potential and in saline sediments (Swan et al., 2010; Hollister et al., of the bacteria that drive particular steps in a biogeochemical 2010), with changes in the abundance of specific functional cycle have not been characterized in this system. groups, such as ammonia-oxidizing (Bernhard et al., 2005) We conducted a metagenomic survey of the Coorong la- and sulfate-reducing bacteria (Oakley et al., 2010), and over- goon as a model for continuous natural salinity and nutrient all composition (Hollister et al., 2010; Swan et al., 2010; gradients, and describe the shifts in gene content of sediment Bouvier and del Giorgio, 2002), suggesting the important se- microbial metagenomes along the salinity gradient from ma- lective role of salinity. However, it is not known how these rine to hypersaline conditions. This provides a model for how taxonomic shifts will change the functional gene content in- environmental gradients can drive shifts in the biogeochem- volved in biogeochemical processes, with the majority of ically important metabolic processes involved in salinity tol- studies focusing on taxonomic marker genes or specific func- erance and in taxonomic groups involved in photosynthesis tional groups. and nitrogen cycling. Metagenomics allows for the elucidation of the biochem- ical potential of microbial genomes present in a given en- vironmental sample via direct sequencing of community 2 Materials and methods DNA (Tyson et al., 2004; Wooley et al., 2010). Several metagenomic studies (Kunin et al., 2008; Rodriguez-Brito 2.1 Study sites and sample collection et al., 2010) have focused on specific hypersaline environ- ments, but there has been no assessment of metabolic shifts Sampling was conducted at four reference stations along the along salinity gradients. Additionally, the majority of non- Coorong lagoon, South Australia, in January 2008, during metagenomic studies have investigated either estuarine habi- the Austral summer. Salinity varied by 99 across stations, tats that do not exceed 50 salinity (Practical Salinity Scale) expressed using the Practical Salinity Scale (Lewis, 1980). or extreme hypersaline environments (e.g. solar salterns). The sites were named by their salinity and defined by their In this context, the Coorong lagoon, in South Australia GPS coordinates, which were as follows: 37 (−35.551◦ S, provides a unique model system of a continuous, natu- 138.883◦ E), 109 (−35.797◦ S, 139.317◦ E), 132 (−35.938S, ral salinity gradient from estuarine to hypersaline salinities 139.488◦ E) & 136 (−36.166◦ S, 139.651◦ E). Ammonia (Lester and Fairweather, 2009; Schapira et al., 2009), which concentrations at these sites ranged between 0.21 (±0.09) provides an opportunity to investigate shifts in the biogeo- and 3.10 (±0.84) mgN l−1, phosphate concentrations ranged chemical potential and function of microbial communities. between 0.05 (±0.01) and 0.27 (±0.09) mgP l−1 (Supple- The Coorong lagoon is one of Australia’s most significant ment
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