Ellen C. Hopmans

Distributional variations in marine crenarchaeotal membrane lipids: a new tool for reconstructing ancient sea water temperatures?

It has recently been shown that membrane lipids of marine crenarchaeota, a ubiquitous and abundant component of plankton, occur in relatively high concentrations in recent and ancient sediments. In this study we investigated the environmental controls on the relative distribution of these lipids in surface sediments. We especially focussed on temperature, as it is known from the thermophilic genetic relatives of marine crenarchaetoa that the composition of their membrane strongly depends on growth temperature. Indeed, a significant linear correlation (r2=0.92) is found between the number of cyclopentane rings in sedimentary membrane lipids derived from marine crenarchaeota and the annual mean sea surface temperatures. This suggests that the mechanism of physical adaptation of their membrane compositions to temperature is identical to that of their thermophilic relatives. In turn, archaeal lipid distributions in sediments may thus allow the reconstruction of sea water temperatures of ancient marine environments.

Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota.

The basic structure and stereochemistry of the characteristic glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipid of cosmopolitan pelagic crenarchaeota has been identified by high field two-dimensional (2D)-NMR techniques. It contains one cyclohexane and four cyclopentane rings formed by internal cyclisation of the biphytanyl chains. Its structure is similar to that of GDGTs biosynthesized by (hyper)thermophilic crenarchaeota apart from the cyclohexane ring. These findings are consistent with the close phylogenetic relationship of (hyper)thermophilic and pelagic crenarchaeota based 16S rRNA. The latter group inherited the biosynthetic capabilities for a membrane composed of cyclopentane ring-containing GDGTs from the (hyper)thermophilic crenarchaeota. However, to cope with the much lower temperature of the ocean, a small but key step in their evolution was the adjustment of the membrane fluidity by making a kink in one of the bicyclic biphytanyl chains by the formation of a cyclohexane ring. This prevents the dense packing characteristic for the cyclopentane ring-containing GDGTs membrane lipids used by hyperthermophilic crenarchaeota to adjust their membrane fluidity to high temperatures.

Analysis of intact tetraether lipids in archaeal cell material and sediments by high performance liquid chromatography/atmospheric pressure chemical ionization mass spectrometry

A method combining normal phase high performance liquid chromatography (HPLC) with positive ion atmospheric pressure chemical ionization mass spectrometry (APCI-MS) was developed for the analysis of intact glycerol dialkyl glycerol tetraethers (GDGTs) in archaeal cell material and sediments. All GDGTs previously reported to occur in the thermophilic archaeon Sulfolobus solfataricus could be identified based on their mass spectra and retention time. Positive ion mass spectra consisted of abundant protonated molecules and fragment ions corresponding to loss of water and the glycerol moiety. In addition, two novel GDGTs representing alternative combinations of biphytanyl moieties were observed. Using this method, the tetraethers present in the thermophilic archaeon Metallosphaera sedula and two sediment samples were characterized. This rapid method will greatly contribute to the establishment of the sedimentary record of these compounds and increase our understanding of archaea and their occurrence in widely different environments.

Northern hemisphere controls on tropical southeast African climate during the past 60,000 years.

The processes that control climate in the tropics are poorly understood. We applied compound-specific hydrogen isotopes (δD) and the TEX86 (tetraether index of 86 carbon atoms) temperature proxy to sediment cores from Lake Tanganyika to independently reconstruct precipitation and temperature variations during the past 60,000 years. Tanganyika temperatures follow Northern Hemisphere insolation and indicate that warming in tropical southeast Africa during the last glacial termination began to increase ∼3000 years before atmospheric carbon dioxide concentrations. δD data show that this region experienced abrupt changes in hydrology coeval with orbital and millennial-scale events recorded in Northern Hemisphere monsoonal climate records. This implies that precipitation in tropical southeast Africa is more strongly controlled by changes in Indian Ocean sea surface temperatures and the winter Indian monsoon than by migration of the Intertropical Convergence Zone.

Linearly concatenated cyclobutane lipids form a dense bacterial membrane.

Lipid membranes are essential to the functioning of cells, enabling the existence of concentration gradients of ions and metabolites. Microbial membrane lipids can contain three-, five-, six- and even seven-membered aliphatic rings, but four-membered aliphatic cyclobutane rings have never been observed. Here we report the discovery of cyclobutane rings in the dominant membrane lipids of two anaerobic ammonium-oxidizing (anammox) bacteria. These lipids contain up to five linearly fused cyclobutane moieties with cis ring junctions. Such ‘ladderane’ molecules are unprecedented in nature but are known as promising building blocks in optoelectronics. The ladderane lipids occur in the membrane of the anammoxosome, the dedicated intracytoplasmic compartment where anammox catabolism takes place. They give rise to an exceptionally dense membrane, a tight barrier against diffusion. We propose that such a membrane is required to maintain concentration gradients during the exceptionally slow anammox metabolism and to protect the remainder of the cell from the toxic anammox intermediates. Our results further illustrate that microbial membrane lipid structures are far more diverse than previously recognized.

13,16-Dimethyl Octacosanedioic Acid (iso-Diabolic Acid), a Common Membrane-Spanning Lipid of Acidobacteria Subdivisions 1 and 3

ABSTRACT The distribution of membrane lipids of 17 different strains representing 13 species of subdivisions 1 and 3 of the phylum Acidobacteria, a highly diverse phylum of the Bacteria, were examined by hydrolysis and gas chromatography-mass spectrometry (MS) and by high-performance liquid chromatography-MS of intact polar lipids. Upon both acid and base hydrolyses of total cell material, the uncommon membrane-spanning lipid 13,16-dimethyl octacosanedioic acid (iso-diabolic acid) was released in substantial amounts (22 to 43% of the total fatty acids) from all of the acidobacteria studied. This lipid has previously been encountered only in thermophilic Thermoanaerobacter species but bears a structural resemblance to the alkyl chains of bacterial glycerol dialkyl glycerol tetraethers (GDGTs) that occur ubiquitously in peat and soil and are suspected to be produced by acidobacteria. As reported previously, most species also contained iso-C15 and C16:1ω7C as major fatty acids but the presence of iso-diabolic acid was unnoticed in previous studies, most probably because the complex lipid that contained this moiety was not extractable from the cells; it could only be released by hydrolysis. Direct analysis of intact polar lipids in the Bligh-Dyer extract of three acidobacterial strains, indeed, did not reveal any membrane-spanning lipids containing iso-diabolic acid. In 3 of the 17 strains, ether-bound iso-diabolic acid was detected after hydrolysis of the cells, including one branched GDGT containing iso-diabolic acid-derived alkyl chains. Since the GDGT distribution in soils is much more complex, branched GDGTs in soil likely also originate from other (acido)bacteria capable of biosynthesizing these components.

Extremely high sea-surface temperatures at low latitudes during the middle Cretaceous as revealed by archaeal membrane lipids

The middle Cretaceous (125-88 Ma) greenhouse world was characterized by high atmospheric CO 2 levels, the general absence of polar ice caps, and much higher global temperatures than at present. Both δ 1 8 O-based and model-based temperature reconstructions indicate extremely high sea-surface temperatures (SSTs) at high latitudes. However, there are a number of uncertainties with SST reconstructions based on δ 1 8 O isotope data of foraminifera due to diagenetic overprinting effects and tenuous assumptions with respect to the δ 1 8 O value of Cretaceous seawater, the paleoecology of middle Cretaceous marine organisms and seawater pH. Here we applied a novel SST proxy (i.e., TEXT [tetraether index of 86 carbon atoms], based on the membrane lipids of marine crenarchaeota) derived from middle Cretaceous sedimentary rocks deposited at low latitudes. The TEXT proxy indicates that tropical SSTs in the proto-North Atlantic were at 32-36 °C during the early Albian and late Cenomanian-early Turonian. This finding agrees with SST estimates based on δ 1 8 O paleothermometry of well-preserved foraminifera as well as global circulation model calculations. The TEXT proxy indicates cooler SSTs (27-32 °C) for the equatorial Pacific during the early Aptian, which is in agreement with SST estimates based on δ 1 8 O paleothermometry.

Archaeal lipids in Mediterranean cold seeps: molecular proxies for anaerobic methane oxidation

Abstract We investigated the distributions and δ13C values of biomarkers for Archaea associated with anaerobic methane oxidation in disparate settings throughout two Eastern Mediterranean mud dome fields. All major classes of archaeal lipids are present in the studied sediments, including isoprenoid glycerol diethers, isoprenoid glycerol dialkyl glycerol tetraethers, and irregular isoprenoid hydrocarbons. Of the compounds present, many, including a novel glycerol tetraether and sn-3-hydroxyarchaeol, have not been previously reported for settings in which methane oxidation is presumed to occur. Archaeal lipids are depleted in 13C, indicating that the Archaea from which they derive are either directly or indirectly involved with methane consumption. The most widespread archaeal lipids are archaeol, PMI, and glycerol tetraethers, and these compounds are present at all active sites. However, archaeal lipid abundances and distributions are highly variable; ratios of crocetane, PMI, and hydroxyarchaeol relative to archaeol vary from 0 to 6.5, from 0 to 2, and from 0 to 1, respectively. These results suggest that archaeal communities differ amongst the sites examined. In addition, carbon isotopic variability amongst archaeal biomarkers in a given mud breccia can be as large as 24 ‰, suggesting that even at single sites multiple archaeal species perform or are supported by anaerobic methane oxidation.

Crenarchaeotal membrane lipids in lake sediments: A new paleotemperature proxy for continental paleoclimate reconstruction?

Paleoclimate studies of continental environments have been hampered by the lack of an independent paleotemperature proxy. A novel sea-surface temperature proxy has been proposed for marine systems based on membrane lipids of marine crenarchaeota. This proxy will provide an independent continental paleotemperature tool that will allow paleoclimatologists to address fundamental questions about temperature variability in continental environments and its relationship to climate change.

Archaea mediate anaerobic oxidation of methane in deep euxinic waters of the Black Sea

We evaluate anaerobic oxidation of methane (AOM) in the Black Sea water column by determining distributions of archaea-specific glyceryl dialkyl glyceryl tetraethers (GDGTs) and 13C isotopic compositions of their constituent biphytanes in suspended particulate matter (SPM), sinking particulate matter collected in sediment traps, and surface sediments. We also determined isotopic compositions of fatty acids specific to sulfate-reducing bacteria to test for biomarker and isotopic evidence of a syntrophic relationship between archaea and sulfate-reducing bacteria in carrying out AOM. Bicyclic and tricyclic GDGTs and their constituent 13C-depleted monocyclic and bicyclic biphytanes (down to −67‰) indicative of archaea involved in AOM were present in SPM in the anoxic zone below 700 m depth. In contrast, GDGT-0 and crenarchaeol derived from planktonic crenarchaeota dominated the GDGT distributions in the oxic surface and shallow anoxic waters. Fatty acids indicative of sulfate-reducing bacteria (i.e., iso- and anteiso-C15) were not strongly isotopically depleted (e.g., −32 to −25‰), although anteiso-C15 was 5‰ more depleted in 13C than iso-C15. Our results suggest that either AOM is carried out by archaea independent of sulfate-reducing bacteria or those sulfate-reducing bacteria involved in a syntrophy with methane-oxidizing archaea constitute a small enough fraction of the total sulfate-reducing bacterial community that an isotope depletion in their fatty acids is not readily detected. Sinking particulate material collected in sediment traps and the underlying sediments in the anoxic zone contained the biomarker and isotope signature of upper–water column archaea. AOM-specific GDGTs and 13C-depleted biphytanes characteristic of the SPM in the deep anoxic zone are not incorporated into sinking particles and are not efficiently transported to the sediments. This observation suggests that sediments may not always record AOM in overlying euxinic water columns and helps explain the absence of AOM-derived biomarkers in sediments deposited during past periods of elevated levels of methane in the ocean.