Crenarchaeol dominates the membrane lipids of Candidatus Nitrososphaera gargensis, a thermophilic Group I.1b Archaeon

Abstract

Analyses of archaeal membrane lipids are increasingly being included in ecological studies as a comparatively unbiased complement to gene-based microbiological approaches. For example, crenarchaeol, a glycerol dialkyl glycerol tetraether (GDGT) with a unique cyclohexane moiety, has been postulated as biomarker for ammonia-oxidizing Archaea (AOA). Crenarchaeol has been detected in Nitrosopumilus maritimus and ‘Candidatus Nitrosocaldus yellowstonii’ representing two of the three lineages within the Crenarchaeota containing described AOA. In this paper we present the membrane GDGT composition of ‘Candidatus Nitrososphaera gargensis’, a moderately thermophilic AOA, and the only cultivated Group I.1b Crenarchaeon. At a cultivation temperature of 46 °C, GDGTs of this organism consisted primarily of crenarchaeol, its regioisomer, and a novel GDGT. Intriguingly, ‘Ca. N. gargensis’ is the first cultivated archaeon to synthesize substantial amounts of the crenarchaeol regioisomer, a compound found in large relative abundances in tropical ocean water and some soils, and an important component of the TEX86 paleothermometer. Intact polar lipid (IPL) analysis revealed that ‘Ca. N. gargensis’ synthesizes IPLs similar to those reported for the Goup I.1a AOA, Nitrosopumilus maritimus SCMI, in addition to IPLs containing uncharacterized headgroups. Overall, the unique GDGT composition of ‘Ca. N. gargensis’ extends the known taxonomic distribution of crenarchaeol synthesis to the Group I.1b Crenarchaeota, implicating this clade as a potentially important source of crenarchaeol in soils and moderately high temperature environments. Moreover, this work supports the hypothesis that crenarchaeol is specific to all AOA and highlights specific lipids, which may prove useful as biomarkers for ‘Ca. N. gargensis’-like AOA.

A robust nitrifying community in a bioreactor at 50 °C opens up the path for thermophilic nitrogen removal

“…Isotopic analysis of the biphytane moieties of the characteristic archaeal membrane lipids, GDGTs (glycerol dibiphytanyl glycerol tetraether lipids), was performed for AOAs. The GDGTs were dominated by crenarchaeol, in agreement with culture studies of 'Candidatus Nitrososphaera gargensis' (Pitcher et al, 2010). The two biphytanes released showed considerable enrichment in 13 C compared with the start of the incubation, pointing at AOA autotrophy (Figure 4).…”

“…The presence of the described core nitrifiers in the bioreactor was, furthermore, linked with their activity and functionality. Incorporation of 13 C-labeled bicarbonate was observed into crenarchaeol and 11-methyl C16:0, characteristic membrane lipids for 'Candidatus Nitrososphaera gargensis' (Pitcher et al, 2010) and Nitrospira (Lipski et al, 2001), respectively. Although the carbon assimilation confirmed the autotrophic activity of the studied nitrifiers, it does not exclude the presence of other, unknown autotrophic or heterotrophic nitrifiers.…”

Differential degradation of intact polar and core glycerol dialkyl glycerol tetraether lipids upon post-depositional oxidation

“…Analysis of the unoxidized sediment showed the presence of two main intact polar lipid species, MH crenarchaeol and DH crenarchaeol, while no HPH crenarchaeol was detected. This distribution is different from the distribution in cultures, where HPH crenarchaeol is always present Pitcher et al, 2010;Pitcher et al, 2011b;Sinninghe Damsté et al, 2012) but is similar to that of IPLs in deeper marine sediments (Biddle et al, 2006;Lipp and Hinrichs, 2009). The absence of HPH crenarchaeol is probably due to the greater lability of this IPL GDGT, as shown for Arabian Sea sediments, where degradation at the surface occurred within a few cm (Lengger et al, 2012b).…”

“…Due to a lack of standards, the results are reported as arbitrary area unit (aau). Signal stability was monitored using a lipid extract of Candidatus Nitrososphaera gargensis (Pitcher et al, 2010) that was injected every 8 runs. Quantification of IPL concentration was done based on results from preparative HPLC.…”

Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids in the Arabian Sea oxygen minimum zone. Part II: Selective preservation and degradation in sediments and consequences for the TEX86

“…Most of the cultivated Crenarchaeota and Thaumarchaeota produce tetraether lipids consisting of two back-to-back linked diethers (glycerol dibiphytanyl glycerol tetraethers, GDGTs) which can have varying numbers of cyclopentane moieties (Macalady et al, 2004;Koga and Morii, 2005;Schouten et al, 2008;Pitcher et al, 2010). Thaumarchaeota contain in addition a specific GDGT, crenarchaeol, which contains not only cyclopentane moieties but also one cyclohexane moiety (Sinninghe Damsté et al, 2002b).…”