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. 2015 Dec;9(12):2740-4.
doi: 10.1038/ismej.2015.77. Epub 2015 May 22.

Metabolic Potential of Fatty Acid Oxidation and Anaerobic Respiration by Abundant Members of Thaumarchaeota and Thermoplasmata in Deep Anoxic Peat

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Metabolic Potential of Fatty Acid Oxidation and Anaerobic Respiration by Abundant Members of Thaumarchaeota and Thermoplasmata in Deep Anoxic Peat

Xueju Lin et al. ISME J. .
Free PMC article

Abstract

To probe the metabolic potential of abundant Archaea in boreal peats, we reconstructed two near-complete archaeal genomes, affiliated with Thaumarchaeota group 1.1c (bin Fn1, 8% abundance), which was a genomically unrepresented group, and Thermoplasmata (bin Bg1, 26% abundance), from metagenomic data acquired from deep anoxic peat layers. Each of the near-complete genomes encodes the potential to degrade long-chain fatty acids (LCFA) via β-oxidation. Fn1 has the potential to oxidize LCFA either by syntrophic interaction with methanogens or by coupling oxidation with anaerobic respiration using fumarate as a terminal electron acceptor (TEA). Fn1 is the first Thaumarchaeota genome without an identifiable carbon fixation pathway, indicating that this mesophilic phylum encompasses more diverse metabolisms than previously thought. Furthermore, we report genetic evidence suggestive of sulfite and/or organosulfonate reduction by Thermoplasmata Bg1. In deep peat, inorganic TEAs are often depleted to extremely low levels, yet the anaerobic respiration predicted for two abundant archaeal members suggests organic electron acceptors such as fumarate and organosulfonate (enriched in humic substances) may be important for respiration and C mineralization in peatlands.

Figures

Figure 1
Figure 1
Maximum likelihood tree based on SSU rRNA gene sequences. Solid triangles, sequences retrieved from assembled contigs; open triangles, sequences reconstructed by EMIRGE (Expectation maximization iterative reconstruction of genes from the environment, see Supplementary methods). Numbers in parentheses indicate the percentage of sequences or read coverage.
Figure 2
Figure 2
Metabolic reconstruction of central carbon metabolism, electron transport chains, energy conservation pathways and ABC transporters deduced from Thaumarchaeota Fn1 and Thermoplasmata Bg1 genomes. Shared functions and intermediates are shown in black color. Blue and red colors highlighted those only found in Fn1 and Bg1, respectively. Dotted lines indicate possible electron flow for the Fn1 and Bg1 populations. Dashed lines indicate putative reactions or proton movement across the membrane. Gray arrows indicate missing functions. Numbers correspond to enzymes: 1, phosphoglucomutase; 2, glucokinase; 3, glucose-6-phosphate isomerase; 4, fructose-1,6-bisphosphatase; 5, 6-phosphofructokinase; 6, fructose-bisphosphate aldolase, class I; 7, glyceraldehyde-3-phosphate dehydrogenase (NAD(P)); 8, phosphoglycerate kinase; 9, 2,3-bisphosphoglycerate-independent phosphoglycerate mutase; 10, enolase; 11, pyruvate kinase; 12, pyruvate ferredoxin oxidoreductase; 13, AMP-type acetyl-CoA synthetase; 14, phosphoenolpyruvate carboxykinase; 15, pyruvate carboxylase; 16, citrate synthase; 17, aconitate hydratase; 18, isocitrate dehydrogenase (NAD+); 19, 2-oxoglutarate ferredoxin oxidoreductase subunit alpha; 20, succinyl-CoA synthetase alpha subunit; 21, succinate dehydrogenase (ubiquinone) flavoprotein subunit; 22, fumarate hydratase; 23, malate dehydrogenase; 24, acetyl-CoA C-acetyltransferase; 25, aldehyde dehydrogenase (NAD+); 26, alcohol dehydrogenase; 27, transketolase; 28, ribulose-phosphate 3-epimerase; 29, ribose 5-phosphate isomerase; 30, ribose-phosphate pyrophosphokinase; 31, long-chain acyl-CoA synthetase; 32, acyl-coA dehydrogenase; 33, Enoyl-CoA hydratase; 34, 3-hydroxyacyl-CoA dehydrogenase; 35, 3-ketoacyl-CoA thiolase; 36, NADH-quinone oxidoreductase; 37, Succinate dehydrogenase/fumarate reductase; 38, ubiquinol-cytochrome c reductase; 39, F-type H+-transporting ATPase; 40, inorganic pyrophosphatase; 41, sulfate adenylyltransferase; 42, thiosulfate sulfurtransferase; 43, sulfur:oxygen oxidoreductase; 44, dissimilatory sulfite reductase. EC# for each enzyme is listed in Supplementary Table S2. Information on gene annotation, length, and annotation sources are listed in the Supplementary files ‘Supplementary information of genes annotated for the Fn1 genome.pdf' and ‘Supplementary information of genes annotated for the Bg1 genome.pdf'.

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