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Aciduliprofundum Boonei’’, a Cultivated Obligate Thermoacidophilic Euryarchaeote from Deep-Sea Hydrothermal Vents

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Aciduliprofundum Boonei’’, a Cultivated Obligate Thermoacidophilic Euryarchaeote from Deep-Sea Hydrothermal Vents Extremophiles (2008) 12:119–124 DOI 10.1007/s00792-007-0111-0 ORIGINAL PAPER Tetraether membrane lipids of Candidatus ‘‘Aciduliprofundum boonei’’, a cultivated obligate thermoacidophilic euryarchaeote from deep-sea hydrothermal vents Stefan Schouten Æ Marianne Baas Æ Ellen C. Hopmans Æ Anna-Louise Reysenbach Æ Jaap S. Sinninghe Damste´ Received: 11 June 2007 / Accepted: 28 August 2007 / Published online: 28 September 2007 Ó Springer 2007 Abstract The lipid composition of Candidatus ‘‘Acidu- vents contain ecosystems, which are predominantly fueled liprofundum boonei’’, the only cultivated representative of by geochemical energy and are host to many newly archaea falling in the DHVE2 phylogenetic cluster, a group described free-living microbes, which are often associated of microorganisms ubiquitously occurring at hydrothermal with actively venting porous deep-sea vent deposits or vents, was studied. The predominant core membrane lipids ‘‘chimneys’’. The steep chemical and thermal gradients in this thermophilic euryarchaeote were found to be com- within the walls of these deposits provide a wide range of posed of glycerol dibiphytanyl glycerol tetraethers microhabitats for microorganisms with suitable conditions (GDGTs) containing 0–4 cyclopentyl moieties. In addition, for aerobic and anaerobic thermophiles and mesophiles GDGTs with an additional covalent bond between the (e.g. McCollom and Schock 1997). Indeed, both culture- isoprenoid hydrocarbon chains, so-called H-shaped dependent and -independent approaches have exposed a GDGTs, were present. The latter core lipids have been vast diversity of Bacteria and Archaea associated with rarely reported previously. Intact polar lipid analysis deep-sea vent deposits (e.g. Reysenbach and Shock 2002; revealed that they predominantly consist of GDGTs with a Schrenk et al. 2003). Numerous Archaea have been iso- phospho-glycerol headgroup. lated from these deposits but few of these are found in environmental 16S rRNA gene clone libraries and most Keywords Aciduliprofundum boonei Á DHVE2 cluster Á detected environmental clones in these environments have Glycerol dialkyl glycerol tetraethers Á Thermoacidophile no representatives available in pure culture. In particular, one archaeal lineage is widespread at deep- sea vents, namely the ‘‘deep-sea hydrothermal vent eury- Introduction archaeotic’’ lineage DHVE2, and is frequently associated with actively venting sulphide deposits (e.g. Nercessian Deep-sea hydrothermal vents are unique environments, et al. 2003; Hoek et al. 2003; Reysenbach and Shock 2002; which are thought to represent models for both the origin of Takai et al. 1999, 2001). In some cases it has been reported life on Earth and exploration of life on other planets. These as the most dominant clone type in archaeal clone libraries (Hoek et al. 2003), yet the physiology of these organisms was unclear. Recently, Reysenbach et al. (2006) isolated Communicated by J. N. Reeve. and cultivated a member of the DHVE2 phylogenetic DHVE2 cluster, Candidatus ‘‘Aciduliprofundum boonei’’, & S. Schouten ( ) Á M. Baas Á E. C. Hopmans Á J. S. S. Damste´ and showed it to be an obligate thermoacidophilic sulphur Department of Marine Biogeochemistry and Toxicology, Royal Netherlands Institute for Sea Research, PO Box 59, and iron reducing heterotroph capable of growing from 1790 AB Den Burg, Texel, The Netherlands pH 3.3 to 5.8 and between 60 and 75°C. This provided the e-mail: [email protected] first evidence that thermoacidophiles may be key players in sulphur and iron cycling at deep-sea vents. A.-L. Reysenbach Department of Biology, Portland State University, Portland, Archaea are not only unique in their 16S rRNA phylo- OR 97201, USA genetic position in the tree of life, but also synthesize 123 120 Extremophiles (2008) 12:119–124 specific membrane lipids. Analysis of cultivated hyper- Materials and methods thermophilic Archaea showed that their membrane is predominantly composed of isoprenoid glycerol dib- Culture conditions iphytanyl glycerol tetraethers (GDGTs) with additional cyclopentyl moieties (e.g. Structures I–VI in Fig. 1). The Aciduliprofundum boonei was grown as previously structural differences from diacyl membrane lipids of non- described (Reysenbach et al. 2006). Cells were harvested at thermophilic Eukarya and Bacteria, i.e. ether bonds and the late log phase of growth. Cell pellets were freeze-dried and formation of a monolayer rather than a bilayer, have been stored frozen until analysis. suggested to contribute to the stability of membranes of hyperthermophiles at high temperatures and low pH (e.g. De Rosa and Gambacorta 1988; van den Vossenberg et al. Core lipid analysis 1998; Macalady et al. 2004). This suggests that members of the DHVE2 cluster may be also synthesizing GDGT Cell material (74 mg dry weight) of A. boonei was membrane lipids. Therefore, in this study we analyzed the hydrolyzed by refluxing in ca. 4 ml 1 M KOH in methanol lipid composition of the only cultivated representative of for 1 h. The pH of the hydrolyzed extract was adjusted to DHVE2, Aciduliprofundum boonei, and examined both the pH 3 using 2 M HCl/methanol (MeOH) 1/1 (v/v) and core GDGT lipid composition as well as its intact polar transferred to a separatory funnel. The residual cell mate- lipid composition. rial was washed subsequently with 2 ml MeOH/water Fig. 1 HPLC/APCI/MS base II peak chromatogram of GDGT core lipids in extract released after base hydrolysis (using KOH/methanol mixture) of the cell material of Candidatus ‘‘Aciduliprofundum boonei’’. iy [M+H]+ 1300 Inset shows the atmospheric tnst 100 i c pressure chemical ionization e a 80 d n mass spectrum of GDGT VII. u b 60 ltiven A e Note that the position of the e vn Ra 40 a covalent bond between the lie Re t 20 isoprenoid hydrocarbon chains 1282 1226 in GDGTs VII–XI is tentative 0 (Morii et al. 1998) 900 1000 1100 1200 1300 1400 III m/z IV VI V VII I VIII IX X XI Relative retention time HO HO O O I O O O O O VII O HO OH OH HO O O O O II O O OH HO VIII O O O HO OH O III O O O IX O O OH HO O O HO OH IV O O O O X O O HO OH HO O O O OH V O O XI O O O HO OH O VI O OH O O O OH 123 Extremophiles (2008) 12:119–124 121 1/1 (v/v), MeOH and dichloromethane (DCM, three times). chromatography manager software. Separation was The washings and 6 ml bidistilled water were added to the achieved on a Prevail Cyano column (2.1 · 150 mm, separatory funnel, which was shaken vigorously. The DCM 3 lm; Alltech, Deerfield, IL, USA), maintained at 30°C. layer was removed and the residual water/MeOH layer was Injection volumes were 10 ll. GDGTs were eluted iso- re-extracted two times using DCM. The combined DCM cratically with 99% A and 1% B for 5 min, followed by a layers were dried using a sodium sulfate column to yield linear gradient to 1.8% B in 45 min, where A = hexane and the hydrolyzed extract. The extract released upon hydro- B = isopropanol. Flow rate was 0.2 ml/min. After each lysis was condensed by rotary evaporation. Elemental analysis the column was cleaned by back-flushing hexane/ sulphur was removed with activated Cu. The extract was isopropanol (90:10, v/v) at 0.2 ml/min for 10 min. Detec- methylated by diazomethane and filtered over a silicagel tion was achieved using atmospheric pressure positive ion column using ethyl acetate. One aliquot of the eluate was chemical ionization mass spectrometry (APCI-MS) of the silylated using BSTFA (with 1% TMCS) in pyridine (1/1, eluent. Conditions for the HP 1100 APCI-MSD SL were as v/v) for 20 min at 60°C and subsequently analyzed by gas follows: nebulizer pressure 60 psi, vaporizer temperature chromatography (GC) and GC/mass spectrometry (GC/ 400°C, drying gas (N2) flow 6 l/min and temperature MS). Another aliquot of the eluate was dissolved in hex- 200°C, capillary voltage –3 kV, corona 5 lA(*3.2 kV). ane/isopropanol (99:1, v/v), ultrasonicated and filtered GDGTs were detected by mass scanning from m/z 950– using a PTFE 0.45-lm filter prior to analysis for GDGTs 1,450. on the high performance liquid chromatography (HPLC)/ MS. Part of the GDGT fraction was hydrogenated by dis- Intact polar lipid analysis solving it in ethyl acetate, adding a small amount of PtO2 and a drop of acetic acid and bubbling hydrogen for 1 h. For analysis of the intact polar lipids, cell material of Subsequently, the solution was stirred overnight and fil- A. boonei were extracted using a modified Bligh–Dyer tered over a small pipette column containing Na2CO3 (top) procedure (Bligh and Dyer 1959). To an aliquot of the cell and MgSO4 (bottom). Ethyl acetate was evaporated and the material, a solvent mixture of phosphate-buffer (0.05 M, hydrogenated GDGT fraction was dissolved in hexane/ pH 7.4)/MeOH/DCM 0.8/2/1 (v/v) was added. The mixture isopropanol (99:1, v/v), ultrasonicated and analyzed using was sonicated for 10 min after which DCM and phosphate HPLC/MS. buffer were added to a volume ratio of 0.9/l/1. After cen- A second aliquot of the GDGT fraction was separated trifuging (2,500 rpm, 5 min) the DCM layer was collected. using HPLC with a preparative device (Foxy jr) and the The residue was re-extracted twice following the same fractions collected were analyzed by flow injection analysis procedure. The combined DCM layers were concentrated mass spectrometry (Smittenberg et al. 2002). The fractions by evaporating solvent under a N2 stream, dried with containing the unusual GDGT (see text below) were Na2SO4 and the solvent was removed under a N2 stream.
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