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Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota.

ABSTRACT: Marine ammonia-oxidizing archaea (AOA) are among the most abundant of marine microorganisms, spanning nearly the entire water column of diverse oceanic provinces. Historical patterns of abundance are preserved in sediments in the form of their distinctive glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids. The correlation between the composition of GDGTs in surface sediment and the overlying annual average sea surface temperature forms the basis for a paleotemperature proxy (TEX86) that is used to reconstruct surface ocean temperature as far back as the Middle Jurassic. However, mounting evidence suggests that factors other than temperature could also play an important role in determining GDGT distributions. We here use a study set of four marine AOA isolates to demonstrate that these closely related strains generate different TEX86-temperature relationships and that oxygen (O2) concentration is at least as important as temperature in controlling TEX86 values in culture. All of the four strains characterized showed a unique membrane compositional response to temperature, with TEX86-inferred temperatures varying as much as 12 °C from the incubation temperatures. In addition, both linear and nonlinear TEX86-temperature relationships were characteristic of individual strains. Increasing relative abundance of GDGT-2 and GDGT-3 with increasing O2 limitation, at the expense of GDGT-1, led to significant elevations in TEX86-derived temperature. Although the adaptive significance of GDGT compositional changes in response to both temperature and O2 is unclear, this observation necessitates a reassessment of archaeal lipid-based paleotemperature proxies, particularly in records that span low-oxygen events or underlie oxygen minimum zones.

SUBMITTER: Qin W

PROVIDER: S-EPMC4568219 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota.

Qin Wei W Carlson Laura T LT Armbrust E Virginia EV Devol Allan H AH Moffett James W JW Stahl David A DA Ingalls Anitra E AE

Proceedings of the National Academy of Sciences of the United States of America 20150817 35

Marine ammonia-oxidizing archaea (AOA) are among the most abundant of marine microorganisms, spanning nearly the entire water column of diverse oceanic provinces. Historical patterns of abundance are preserved in sediments in the form of their distinctive glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids. The correlation between the composition of GDGTs in surface sediment and the overlying annual average sea surface temperature forms the basis for a paleotemperature proxy (TEX86) ...[more]

PMID: 26283385

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Project description:Ammonia oxidation regulates the balance of reduced and oxidized nitrogen pools in nature. Although ammonia-oxidizing archaea have been recently recognized to often outnumber ammonia-oxidizing bacteria in various environments, the contribution of ammonia-oxidizing archaea is still uncertain due to difficulties in the in situ quantification of ammonia oxidation activity. Nitrogen and oxygen isotope ratios of nitrite (?(15)NNO2- and ?(18)ONO2-, respectively) are geochemical tracers for evaluating the sources and the in situ rate of nitrite turnover determined from the activities of nitrification and denitrification; however, the isotope ratios of nitrite from archaeal ammonia oxidation have been characterized only for a few marine species. We first report the isotope effects of ammonia oxidation at 70°C by thermophilic Thaumarchaeota populations composed almost entirely of "Candidatus Nitrosocaldus." The nitrogen isotope effect of ammonia oxidation varied with ambient pH (25‰ to 32‰) and strongly suggests the oxidation of ammonia, not ammonium. The ?(18)O value of nitrite produced from ammonia oxidation varied with the ?(18)O value of water in the medium but was lower than the isotopic equilibrium value in water. Because experiments have shown that the half-life of abiotic oxygen isotope exchange between nitrite and water is longer than 33 h at 70°C and pH ?6.6, the rate of ammonia oxidation by thermophilic Thaumarchaeota could be estimated using ?(18)ONO2- in geothermal environments, where the biological nitrite turnover is likely faster than 33 h. This study extended the range of application of nitrite isotopes as a geochemical clock of the ammonia oxidation activity to high-temperature environments.Because ammonia oxidation is generally the rate-limiting step in nitrification that regulates the balance of reduced and oxidized nitrogen pools in nature, it is important to understand the biological and environmental factors underlying the regulation of the rate of ammonia oxidation. The discovery of ammonia-oxidizing archaea (AOA) in marine and terrestrial environments has transformed the concept that ammonia oxidation is operated only by bacterial species, suggesting that AOA play a significant role in the global nitrogen cycle. However, the archaeal contribution to ammonia oxidation in the global biosphere is not yet completely understood. This study successfully identified key factors controlling nitrogen and oxygen isotopic ratios of nitrite produced from thermophilic Thaumarchaeota and elucidated the applicability and its limit of nitrite isotopes as a geochemical clock of ammonia oxidation rate in nature. Oxygen isotope analysis in this study also provided new biochemical information on archaeal ammonia oxidation.

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Dataset Information

Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota.

Publications

Confounding effects of oxygen and temperature on the TEX86 signature of marine Thaumarchaeota.

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