Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates

Elling, Felix J.; Könneke, Martin; Mußmann, Marc; Greve, Andreas; Hinrichs, Kai‐Uwe

doi:10.1016/j.gca.2015.09.004

Cited by 149 publications

(172 citation statements)

References 110 publications

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“…Remarkably, mesophilic Thaumarchaeota and thermophilic Archaea seem to use the same mechanism, GDGT cyclization, to regulate membrane fluidity and proton permeability (21,22,37,38,47). At the depth of maximum thaumarchaeal activity, between 50 and 200 m (e.g., 7, 10), most ocean waters have temperatures between 5 and 15°C (with the exception of polar latitudes).…”

Section: Discussionmentioning

confidence: 99%

“…In our experiments with N. maritimus, the chemostat not only controls the growth and corresponding ammonia oxidation rate but also maintains the thermal and chemical stability of the growth conditions. This approach is fundamentally different from all previous batch culture (21,22,35) and mesocosm (19,20) studies of GDGT-producing planktonic Archaea, in which several potentially competing variables such as metabolic activity, temperature, community assemblage, and chemical composition of the medium simultaneously could have influenced the lipid distributions.…”

Section: Significancementioning

confidence: 93%

“…Indeed, previous studies indicate that GDGT composition may significantly vary even between different strains of cultured planktonic Thaumarchaeota (21,22). The transition from shallowwater to deep-water thaumarchaeal ecotypes has been invoked to explain different relative GDGT compositions through the water column (e.g., refs.…”

Section: Cellular Energy Balance and The Synthesis Of Gdgts: The Redumentioning

confidence: 99%

“…Culture studies have shown that the average number of cyclopentyl moieties in GDGTs can increase with growth temperature in marine Archaea (19)(20)(21)(22); however, TEX 86 values of suspended particulate material (SPM) through the water column do not reflect in situ temperatures either in trend or in magnitude (23)(24)(25)(26)(27)(28)(29). TEX 86 -calculated temperatures in sinking particles and core-top sediments are often colder than mean annual average, especially in highly productive regions such as upwelling systems (30)(31)(32)(33).…”

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confidence: 99%

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Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Hurley

Elling

Könneke

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Archaeal membrane lipids known as glycerol dibiphytanyl glycerol tetraethers (GDGTs) are the basis of the TEX 86 paleotemperature proxy. Because GDGTs preserved in marine sediments are thought to originate mainly from planktonic, ammonia-oxidizing Thaumarchaeota, the basis of the correlation between TEX 86 and sea surface temperature (SST) remains unresolved: How does TEX 86 predict surface temperatures, when maximum thaumarchaeal activity occurs below the surface mixed layer and TEX 86 does not covary with in situ growth temperatures? Here we used isothermal studies of the model thaumarchaeon Nitrosopumilus maritimus SCM1 to investigate how GDGT composition changes in response to ammonia oxidation rate. We used continuous culture methods to avoid potential confounding variables that can be associated with experiments in batch cultures. The results show that the ring index scales inversely (R 2 = 0.82) with ammonia oxidation rate (ϕ), indicating that GDGT cyclization depends on available reducing power. Correspondingly, the TEX 86 ratio decreases by an equivalent of 5.4°C of calculated temperature over a 5.5 fmol·cell −1 ·d −1 increase in ϕ. This finding reconciles other recent experiments that have identified growth stage and oxygen availability as variables affecting TEX 86 . Depth profiles from the marine water column show minimum TEX 86 values at the depth of maximum nitrification rates, consistent with our chemostat results. Our findings suggest that the TEX 86 signal exported from the water column is influenced by the dynamics of ammonia oxidation. Thus, the global TEX 86 -SST calibration potentially represents a composite of regional correlations based on nutrient dynamics and global correlations based on archaeal community composition and temperature.T he glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids of Archaea are abundant in marine water columns and sediments. The major source of GDGTs to ocean sediments is thought to be planktonic, ammonia-oxidizing Archaea (AOA) affiliated with the phylum Thaumarchaeota (formerly Marine Group I Crenarchaeota) (1, 2). Thaumarchaeota play a primary role in the nitrogen cycle, performing the first and rate-limiting step of nitrification-namely, the oxidation of ammonia to nitrite (3-5). Accordingly, Thaumarchaeota are most abundant at the base of, or below, the euphotic zone (6-9). Based on the phylogeny of their ammonia monooxygenase gene, the planktonic Thaumarchaeota are divided into two distinct clusters, the Water Column Cluster A that is most abundant in the epi-and upper mesopelagic (above ∼200 to ∼500 m, depending on location) and the Water Column Cluster B that dominates thaumarchaeal assemblages in the deeper mesopelagic and bathypelagic (7-10). These clusters putatively represent thaumarchaeal ecotypes adapted to high and low ammonium flux, respectively (11,12).Thaumarchaeota produce GDGTs containing from zero to four cyclopentane rings (GDGT-0 to GDGT-4) or four cyclopentane rings and one additional cyclohexane ring (e.g., in crenarchaeol;...

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 93%

Section: Cellular Energy Balance and The Synthesis Of Gdgts: The Redumentioning

confidence: 99%

mentioning

confidence: 99%

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Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Hurley

Elling

Könneke

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

139

142

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“…This traditional viewpoint was thoroughly challenged and changed on the basis of the discovery of AOA. So far, more than 10 strains of AOA were already isolated, and more than 10 enrichments have been cultivated (Blainey et al, 2011;De La Torre et al, 2008;Elling et al, 2015;Hallam et al, 2006;Hatzenpichler et al, 2008;Jung et al, 2011;Jung et al, 2014;Kim et al, 2012;Kim et al, 2016;Könneke et al, 2005;Lehtovirta-Morley et al, 2011;Lehtovirta-Morley et al, 2016a;Mosier et al, 2012;Qin et al, 2014;Sauder et al, 2017). Yet more than 80% of the AOA were still undiscovered so far (Biller et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Potential correlated environmental factors leading to the niche seg- regation of ammonia-oxidizing archaea and ammonia-oxidizing bac- teria: A review

Liu¹,

Hu²,

Shen³

et al. 2017

Appl Env Biotechnol

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Ammonia oxidation is an important step of the nitrogen cycle and was considered to be conducted only by ammonia-oxidizing bacteria (AOB) for a long time. The discovery of ammonia-oxidizing archaea (AOA) caused consideration of the relative contributions of these two functional groups in different niches and factors resulting in their niche segregation. Previous studies showed that some environmental factors may correlate to the abundance and distribution of AOA and AOB, including ammonia/ammonium concentration, pH, organic matters, oxygen concentration, temperature, salinity, sulfide concentration, phosphate concentration, soil moisture and so on. Despite extensive studies conducted on ecology of AOA and AOB to find key environmental factors dominating niche segregation between AOA and AOB, few studies were conducted to explore the interrelationship among environmental factors. In this review, five main environmental factors which may be related to each other were selectively reviewed independently, including ammonia concentration, pH, temperature, oxygen concentration and organic matters. Furthermore, potential interrelationship among environmental factors was proposed.

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Ring Index: A new strategy to evaluate the integrity of TEX₈₆ paleothermometry

2016

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The TEX 86 (tetraether index of 86 carbon atoms) sea surface temperature proxy has been increasingly applied in the reconstruction of Mesozoic and Cenozoic ocean temperatures. However, the archaeal lipids that compose TEX 86 indices, glycerol dialkyl glycerol tetraethers (GDGTs), can derive from water column production, terrestrial sources, and/or within sediments. TEX 86 -sea surface temperature estimates can also be influenced by non-temperature factors, such as growth phase and nutrient levels. Here we show that the weighted average of cyclopentane moieties, known as the Ring Index (RI), can be used to determine if TEX 86 temperature estimates are influenced by non-thermal factors and/or deviate from modern analogues. We demonstrate that RI and TEX 86 indices from the published global core top data set and mesocosm cultures are significantly correlated, as predicted through the influence of temperature on lipid biochemistry. We further show that when RI and TEX 86 indices in modern or ancient records deviate from the modern global TEX 86 -RI relationship, GDGT distributions are not solely controlled by environmental temperature and/or TEX 86 -based temperature reconstructions are questionable.

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Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates

Cited by 149 publications

References 110 publications

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Potential correlated environmental factors leading to the niche seg- regation of ammonia-oxidizing archaea and ammonia-oxidizing bac- teria: A review

Ring Index: A new strategy to evaluate the integrity of TEX₈₆ paleothermometry

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Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates

Cited by 149 publications

References 110 publications

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX 86 temperature proxy

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX 86 temperature proxy

Potential correlated environmental factors leading to the niche seg- regation of ammonia-oxidizing archaea and ammonia-oxidizing bac- teria: A review

Ring Index: A new strategy to evaluate the integrity of TEX86 paleothermometry

Contact Info

Product

Resources

About

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Influence of ammonia oxidation rate on thaumarchaeal lipid composition and the TEX ₈₆ temperature proxy

Ring Index: A new strategy to evaluate the integrity of TEX₈₆ paleothermometry