Stefan Schouten

Archaeal nitrification in the ocean

Marine Crenarchaeota are the most abundant single group of prokaryotes in the ocean, but their physiology and role in marine biogeochemical cycles are unknown. Recently, a member of this clade was isolated from a sea aquarium and shown to be capable of nitrification, tentatively suggesting that Crenarchaeota may play a role in the oceanic nitrogen cycle. We enriched a crenarchaeote from North Sea water and showed that its abundance, and not that of bacteria, correlates with ammonium oxidation to nitrite. A time series study in the North Sea revealed that the abundance of the gene encoding for the archaeal ammonia monooxygenase alfa subunit (amoA) is correlated with a decline in ammonium concentrations and with the abundance of Crenarchaeota. Remarkably, the archaeal amoA abundance was 1–2 orders of magnitude higher than those of bacterial nitrifiers, which are commonly thought to mediate the oxidation of ammonium to nitrite in marine environments. Analysis of Atlantic waters of the upper 1,000 m, where most of the ammonium regeneration and oxidation takes place, showed that crenarchaeotal amoA copy numbers are also 1–3 orders of magnitude higher than those of bacterial amoA. Our data thus suggest a major role for Archaea in oceanic nitrification.

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.

A microbial consortium couples anaerobic methane oxidation to denitrification

Modern agriculture has accelerated biological methane and nitrogen cycling on a global scale. Freshwater sediments often receive increased downward fluxes of nitrate from agricultural runoff and upward fluxes of methane generated by anaerobic decomposition. In theory, prokaryotes should be capable of using nitrate to oxidize methane anaerobically, but such organisms have neither been observed in nature nor isolated in the laboratory. Microbial oxidation of methane is thus believed to proceed only with oxygen or sulphate. Here we show that the direct, anaerobic oxidation of methane coupled to denitrification of nitrate is possible. A microbial consortium, enriched from anoxic sediments, oxidized methane to carbon dioxide coupled to denitrification in the complete absence of oxygen. This consortium consisted of two microorganisms, a bacterium representing a phylum without any cultured species and an archaeon distantly related to marine methanotrophic Archaea. The detection of relatives of these prokaryotes in different freshwater ecosystems worldwide indicates that the reaction presented here may make a substantial contribution to biological methane and nitrogen cycles.

Subtropical Arctic Ocean temperatures during the Palaeocene/Eocene thermal maximum

The Palaeocene/Eocene thermal maximum, ∼55 million years ago, was a brief period of widespread, extreme climatic warming, that was associated with massive atmospheric greenhouse gas input. Although aspects of the resulting environmental changes are well documented at low latitudes, no data were available to quantify simultaneous changes in the Arctic region. Here we identify the Palaeocene/Eocene thermal maximum in a marine sedimentary sequence obtained during the Arctic Coring Expedition. We show that sea surface temperatures near the North Pole increased from ∼18 °C to over 23 °C during this event. Such warm values imply the absence of ice and thus exclude the influence of ice-albedo feedbacks on this Arctic warming. At the same time, sea level rose while anoxic and euxinic conditions developed in the oceans bottom waters and photic zone, respectively. Increasing temperature and sea level match expectations based on palaeoclimate model simulations, but the absolute polar temperatures that we derive before, during and after the event are more than 10 °C warmer than those model-predicted. This suggests that higher-than-modern greenhouse gas concentrations must have operated in conjunction with other feedback mechanisms—perhaps polar stratospheric clouds or hurricane-induced ocean mixing—to amplify early Palaeogene polar temperatures.

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.

Arctic hydrology during global warming at the Palaeocene/Eocene thermal maximum

The Palaeocene/Eocene thermal maximum represents a period of rapid, extreme global warming ∼55 million years ago, superimposed on an already warm world. This warming is associated with a severe shoaling of the ocean calcite compensation depth and a >2.5 per mil negative carbon isotope excursion in marine and soil carbonates. Together these observations indicate a massive release of 13C-depleted carbon and greenhouse-gas-induced warming. Recently, sediments were recovered from the central Arctic Ocean, providing the first opportunity to evaluate the environmental response at the North Pole at this time. Here we present stable hydrogen and carbon isotope measurements of terrestrial-plant- and aquatic-derived n-alkanes that record changes in hydrology, including surface water salinity and precipitation, and the global carbon cycle. Hydrogen isotope records are interpreted as documenting decreased rainout during moisture transport from lower latitudes and increased moisture delivery to the Arctic at the onset of the Palaeocene/Eocene thermal maximum, consistent with predictions of poleward storm track migrations during global warming. The terrestrial-plant carbon isotope excursion (about -4.5 to -6 per mil) is substantially larger than those of marine carbonates. Previously, this offset was explained by the physiological response of plants to increases in surface humidity. But this mechanism is not an effective explanation in this wet Arctic setting, leading us to hypothesize that the true magnitude of the excursion—and associated carbon input—was greater than originally surmised. Greater carbon release and strong hydrological cycle feedbacks may help explain the maintenance of this unprecedented warmth.

Climatic controls on central African hydrology during the past 20,000 years

Past hydrological changes in Africa have been linked to various climatic processes, depending on region and timescale. Long-term precipitation changes in the regions of northern and southern Africa influenced by the monsoons are thought to have been governed by precessional variations in summer insolation. Conversely, short-term precipitation changes in the northern African tropics have been linked to North Atlantic sea surface temperature anomalies, affecting the northward extension of the Intertropical Convergence Zone and its associated rainbelt. Our knowledge of large-scale hydrological changes in equatorial Africa and their forcing factors is, however, limited. Here we analyse the isotopic composition of terrigenous plant lipids, extracted from a marine sediment core close to the Congo River mouth, in order to reconstruct past central African rainfall variations and compare this record to sea surface temperature changes in the South Atlantic Ocean. We find that central African precipitation during the past 20,000 years was mainly controlled by the difference in sea surface temperatures between the tropics and subtropics of the South Atlantic Ocean, whereas we find no evidence that changes in the position of the Intertropical Convergence Zone had a significant influence on the overall moisture availability in central Africa. We conclude that changes in ocean circulation, and hence sea surface temperature patterns, were important in modulating atmospheric moisture transport onto the central African continent.

Stable warm tropical climate through the Eocene epoch

Earths climate cooled from a period of extreme warmth in the early Eocene Epoch (ca. 50 Ma) to the early Oligocene (ca. 33 Ma), when a large ice cap first appeared on Antarctica. Evidence from the planktonic foraminifer oxygen isotope record in deep-sea cores has suggested that tropical sea-surface temperatures declined by 5-10 degrees over this interval, eventually becoming much cooler than modern temperatures. Here we present paleotemperature estimates from foraminifer isotopes and the membrane lipids of marine Crenarcheota from new drill cores in Tanzania that indicate a warm and generally stable tropical climate over this period. We reinterpret the previously published isotope records in the light of comparative textural analysis of the deep-sea foraminifer shells, which shows that in contrast to the Tanzanian material, they have been diagenetically recrystallized. We suggest that increasingly severe alteration of the deep-sea plankton shells through the Eocene produced a diagenetic overprint on their oxygen isotope ratios that imparts the false appearance of a tropical sea-surface cooling trend. This implies that the long-term Eocene climatic cooling trend occurred mainly at the poles and had little effect at lower latitudes.

Methanotrophic symbionts provide carbon for photosynthesis in peat bogs

Wetlands are the largest natural source of atmospheric methane, the second most important greenhouse gas. Methane flux to the atmosphere depends strongly on the climate; however, by far the largest part of the methane formed in wetland ecosystems is recycled and does not reach the atmosphere. The biogeochemical controls on the efficient oxidation of methane are still poorly understood. Here we show that submerged Sphagnum mosses, the dominant plants in some of these habitats, consume methane through symbiosis with partly endophytic methanotrophic bacteria, leading to highly effective in situ methane recycling. Molecular probes revealed the presence of the bacteria in the hyaline cells of the plant and on stem leaves. Incubation with 13C-methane showed rapid in situ oxidation by these bacteria to carbon dioxide, which was subsequently fixed by Sphagnum, as shown by incorporation of 13C-methane into plant sterols. In this way, methane acts as a significant (10–15%) carbon source for Sphagnum. The symbiosis explains both the efficient recycling of methane and the high organic carbon burial in these wetland ecosystems.