Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics

The ISME Journal (2015) 9, 1648–1661; doi:10.1038/ismej.2014.254; published online 9 January 2015

Title 

Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics

Author

Tomàs Llorens-Marès¹, Shibu Yooseph², Johannes Goll³, Jeff Hoffman⁴, Maria Vila-Costa¹, Carles M Borrego^5,6, Chris L Dupont⁴ and Emilio O Casamayor¹

1. ¹Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes–Spanish Council for Research (CEAB-CSIC), Blanes, Girona, Spain
2. ²Informatics Group, J Craig Venter Institute, San Diego, CA, USA
3. ³Informatics Group, J Craig Venter Institute, Rockville, MD, USA
4. ⁴Microbial and Environmental Genomics Group, J Craig Venter Institute, San Diego, CA, USA
5. ⁵Water Quality and Microbial Diversity, Catalan Institute for Water Research (ICRA), Girona, Spain
6. ⁶Group of Molecular Microbial Ecology, Institute of Aquatic Ecology, University of Girona, Girona, Spain

Correspondence: EO Casamayor or CL Dupont, Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes–Spanish Council for Research (CEAB-CSIC), Accés Cala Sant Francesc, 14, Blanes, Girona 17300, Spain. E-mail: casamayor@ceab.csic.es or Microbial and Environmental Genomics Group, J Craig Venter Institute, San Diego, CA 92037, USA. E-mail: cdupont@jcvi.org

Received 19 March 2014; Revised 17 November 2014; Accepted 24 November 2014
Advance online publication 9 January 2015

Abstract

Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and in silico reconstruction of carbon, nitrogen and sulfur metabolic pathways that were tightly coupled through a few bacterial groups. The potential for nitrogen fixation and denitrification was detected in both autotrophs and heterotrophs, with a major role for nitrogen and carbon fixations in Chlorobiaceae. Campylobacterales accounted for a large percentage of denitrification genes, while Gallionellales were putatively involved in denitrification, iron oxidation and carbon fixation and may have a major role in the biogeochemistry of the iron cycle. Bacteroidales were also abundant and showed potential for dissimilatory nitrate reduction to ammonium. The very low abundance of genes for nitrification, the minor presence of anammox genes, the high potential for nitrogen fixation and mineralization and the potential for chemotrophic CO₂ fixation and CO oxidation all provide potential clues on the anoxic zones functioning. We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments. Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.


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http://www.nature.com/ismej/journal/v9/n7/abs/ismej2014254a.html