Metagenomic evidence for sulfur lithotrophy by Epsilonproteobacteria as the major energy source for primary productivity in a sub-aerial arctic glacial deposit, Borup Fiord Pass

• Published in: Frontiers in Microbiology
• Main Authors: Katherine E Wright, Charles eWilliamson, Stephen E Grasby, John R. Spear, Alexis S Templeton
• Format: Article in Journal/Newspaper
• Language: English
• Published: Frontiers Media S.A. 2013
• Subjects: Epsilonproteobacteria; Metagenome; Photosynthesis; Sulfur; free energy; Arctic; Microbiology; QR1-502; Borup Fiord
• Online Access: https://doi.org/10.3389/fmicb.2013.00063; https://doaj.org/article/d7feb3c12c91452db6ef741bf5ebe68b

We combined free energy calculations and metagenomic analyses of an elemental sulfur (S0) deposit on the surface of Borup Fiord Pass Glacier in the Canadian High Arctic to investigate whether the energy available from different redox reactions in an environment predicts microbial metabolism. Many S, C, Fe, As, Mn and NH4+ oxidation reactions were predicted to be energetically feasible in the deposit, and aerobic oxidation of S0 was the most abundant chemical energy source. Small subunit ribosomal RNA (SSU rRNA) gene sequence data showed that the dominant phylotypes were Sulfurovum and Sulfuricurvum, both Epsilonproteobacteria known to be capable of sulfur lithotrophy. Sulfur redox genes were abundant in the metagenome, but sox genes were significantly more abundant than reverse dsr genes. Interestingly, there appeared to be habitable niches that were unoccupied at the depth of genome coverage obtained. Photosynthesis and NH4+ oxidation should both be energetically favorable, but we found few or no functional genes for oxygenic or anoxygenic photosynthesis, or for NH4+ oxidation by either oxygen (nitrification) or nitrite (anammox). The free energy, SSU rRNA gene and quantitative functional gene data are all consistent with the hypothesis that sulfur-based chemolithoautotrophy by Epsilonproteobacteria (Sulfurovum and Sulfuricurvum) is the main form of primary productivity at this site, instead of photosynthesis. This is despite the presence of 24-hour sunlight, and the fact that photosynthesis is not known to be inhibited by any of the environmental conditions present. This is the first time that Sulfurovum and Sulfuricurvum have been shown to dominate a sub-aerial environment, rather than anoxic or sulfidic settings. We also found that Flavobacteria dominate the surface of the sulfur deposits. We hypothesize that this aerobic heterotroph uses enough oxygen to create a microoxic environment in the sulfur below, where the Epsilonproteobacteria can flourish.