Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation.
Archaea of the phylum Thaumarchaeota are among the most abundant prokaryotes on Earth and are widely distributed in marine, terrestrial, and geothermal environments. All studied Thaumarchaeota couple the oxidation of ammonia at extremely low concentrations with carbon fixation. As the predominant nitrifiers in the ocean and in various soils, ammonia-oxidizing archaea contribute significantly to the global nitrogen and carbon cycles. Here we provide biochemical evidence that thaumarchaeal ammonia oxidizers assimilate inorganic carbon via a modified version of the autotrophic hydroxypropionate/hydroxybutyrate cycle of Crenarchaeota that is far more energy efficient than any other aerobic autotrophic pathway. The identified genes of this cycle were found in the genomes of all sequenced representatives of the phylum Thaumarchaeota, indicating the environmental significance of this efficient CO2-fixation pathway. Comparative phylogenetic analysis of proteins of this pathway suggests that the hydroxypropionate/hydroxybutyrate cycle emerged independently in Crenarchaeota and Thaumarchaeota, thus supporting the hypothesis of an early evolutionary separation of both archaeal phyla. We conclude that high efficiency of anabolism exemplified by this autotrophic cycle perfectly suits the lifestyle of ammonia-oxidizing archaea, which thrive at a constantly low energy supply, thus offering a biochemical explanation for their ecological success in nutrient-limited environments.
Organic Geochemistry Group, MARUM-Center for Marine Environmental Sciences, University of Bremen, 28334 Bremen, Germany;Institut für Chemie und Biologie des Meeres, Oldenburg University, 26111 Oldenburg, Germany;
Martin
M
Könneke
Mikrobiologie, Fakultät Biologie, Freiburg University, 79104 Freiburg, Germany;
Daniel M
DM
Schubert
Mikrobiologie, Fakultät Biologie, Freiburg University, 79104 Freiburg, Germany;
Philip C
PC
Brown
Microbiology Department, Water Technology Center, 76139 Karlsruhe, Germany;
Michael
M
Hügler
Institut für Chemie und Biologie des Meeres, Oldenburg University, 26111 Oldenburg, Germany;
Sonja
S
Standfest
Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, 8093 Zurich, Switzerland; and.
Thomas
T
Schwander
Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, 8093 Zurich, Switzerland; and.
Lennart
L
Schada von Borzyskowski
Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, 8093 Zurich, Switzerland; and.
Tobias J
TJ
Erb
Department of Civil and Environmental Engineering, University of Washington, Seattle, WA 98195.
David A
DA
Stahl
Mikrobiologie, Fakultät Biologie, Freiburg University, 79104 Freiburg, Germany; ivan.berg@biologie.uni-freiburg.de.
Ivan A
IA
Berg
D000105:Acetyl Coenzyme A / Q000378:metabolism; D000332:Aerobiosis / Q000502:physiology*; D000641:Ammonia / Q000378:metabolism*; D001105:Archaea / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism; D052818:Autotrophic Processes / Q000502:physiology*; D057486:Carbon Cycle / Q000502:physiology*; D002245:Carbon Dioxide / Q000378:metabolism*; D004734:Energy Metabolism / Q000235:genetics / Q000502:physiology; D019143:Evolution, Molecular; D006836:Hydro-Lyases / Q000235:genetics / Q000378:metabolism; D010084:Oxidation-Reduction; D010788:Photosynthesis / Q000235:genetics / Q000502:physiology; D010802:Phylogeny
D002245:Carbon Dioxide; D000105:Acetyl Coenzyme A; D000641:Ammonia; C066370:4-hydroxybutyryl-CoA dehydratase; D006836:Hydro-Lyases
Nitrosopumilus maritimus; autotrophy