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

Angela Pitcher; Nicolas Rychlik; Ellen C. Hopmans; Eva Spieck; W. Irene C. Rijpstra; Jort Ossebaar; Stefan Schouten; Michael Wagner; Jaap S. Sinninghe Damste

doi:10.1038/ismej.2009.138

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

Angela Pitcher, Nicolas Rychlik, Ellen C. Hopmans, Eva Spieck, W. Irene C. Rijpstra, Jort Ossebaar, Stefan Schouten, Michael Wagner, Jaap S. Sinninghe Damste

Research output: Contribution to journal › Article › Academic › peer-review

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 degrees 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 TEX(86) 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. The ISME Journal (2010) 4, 542-552; doi:10.1038/ismej.2009.138; published online 24 December 2009

Original language	English
Pages (from-to)	542-552
Number of pages	11
Journal	ISME Journal
Volume	4
Issue number	4
DOIs	https://doi.org/10.1038/ismej.2009.138
Publication status	Published - Apr 2010
Externally published	Yes

Funding

Funding for this research was provided by the Dutch Darwin Institute for Biogeology, the NIOZ Royal Netherlands Institute for Sea Research and DFG German Research Foundation (project SP 667/7-370-1). Elena Lebedeva, University of Moscow, is thanked for providing the original material from which 'Ca. N. gargensis' analyzed in this paper was enriched. Three anonymous reviewers are thanked for providing constructive comments, which led to the improvement of this manuscript.

Funders	Funder number
Dutch Darwin Institute for Biogeology
Royal Netherlands Institute for Sea Research - NIOZ
German Research Foundation (DFG)	667/7-370-1

Keywords

'Ca. Nitrososphaera gargensis'
Crenarchaeota
Ammonia oxidation
Crenarchaeol
Intact polar lipids

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10.1038/ismej.2009.138

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title = "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 degrees 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 TEX(86) 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. The ISME Journal (2010) 4, 542-552; doi:10.1038/ismej.2009.138; published online 24 December 2009",

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author = "Angela Pitcher and Nicolas Rychlik and Hopmans, {Ellen C.} and Eva Spieck and Rijpstra, {W. Irene C.} and Jort Ossebaar and Stefan Schouten and Michael Wagner and Damste, {Jaap S. Sinninghe}",

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AU - Rychlik, Nicolas

AU - Hopmans, Ellen C.

AU - Spieck, Eva

AU - Rijpstra, W. Irene C.

AU - Ossebaar, Jort

AU - Schouten, Stefan

AU - Wagner, Michael

AU - Damste, Jaap S. Sinninghe

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N2 - 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 degrees 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 TEX(86) 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. The ISME Journal (2010) 4, 542-552; doi:10.1038/ismej.2009.138; published online 24 December 2009

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

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Keywords

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