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

Katherine E Wright,John R Spear,Alexis S Templeton,Charles Williamson,Stephen E Grasby

doi:10.3389/fmicb.2013.00063

Abstract

We combined free enenergy 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 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 (dissimilatory sulfite reductase)genes. Interestingly, there appeared to be habitable niches that were unoccupied at the depth of genome coverage obtained. Photosynthesis and oxidation should both be energetically favorable, but we found few or no functional genes for oxygenic or anoxygenic photosynthesis, or for 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-h 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.

Highlights

Microbes use a wide range of redox reactions to obtain energy for growth and have a significant impact on the biogeochemical cycling of elements including carbon, nitrogen, and sulfur (Falkowski et al, 2008)
Our free energy calculations based on the geochemical analysis of the BF09-06 sulfur deposit, the SSU rRNA gene data and the data on functional genes found in the metagenome, strongly establish the hypothesis that the main energy source for primary productivity in the BF09-06 deposit is the oxidation of reduced sulfur species
OVERALL CONCLUSIONS ON METABOLIC PATHWAYS Taking into account the free energy calculations, SSU rRNA gene data and the relative abundance of functional genes in the metagenome, we conclude that several sulfur redox reactions may be significant in this environment

Summary

Introduction

Microbes use a wide range of redox reactions to obtain energy for growth and have a significant impact on the biogeochemical cycling of elements including carbon, nitrogen, and sulfur (Falkowski et al, 2008). Some studies have investigated this question by environmental analysis of the small subunit ribosomal RNA (SSU rRNA) gene (Macur et al, 2004; Spear et al, 2005; Costa et al., 2009; Gaidos et al, 2009; Vick et al, 2010) This analysis is limited by our incomplete knowledge of the types of energy metabolism used by each phylotype. Another option is to use the polymerase chain reaction (PCR) to amplify genes for enzymes known to catalyze energy-releasing redox reactions (Hall et al, 2008; Chen et al, 2009; Flores et al, 2011). Metagenomic and metatranscriptomic studies that investigate the relationship between geochemistry, energy sources, and microbial function have already been carried out on a range of different sites including ocean environments (Walsh et al, 2009; Canfield et al, 2010), Yellowstone hot springs (Inskeep et al, 2010), acidic www.frontiersin.org

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