Factors controlling the lipid composition of marine planktonic Thaumarchaeota

Marine ammonia-oxidizing archaea of the phylum Thaumarchaeota synthesize glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids that are used as for the reconstruction of sea surface temperatures by means of the TEX86 paleothermometer. Discrepancies between observed and predicted TEX86-temperatures throughout the global ocean indicate that the physiological and ecological controls on lipid composition in planktonic Thaumarchaeota remain poorly understood. In this thesis, the influence of growth phase, temperature, pH, and salinity on the membrane lipid composition of Thaumarchaeota were investigated. The results indicate that TEX86 is not only influenced by temperature but similarly by growth phase and community composition, which compromises its utility as a paleothermometer. A comprehensive study of the lipidomes of 11 thaumarchaeal cultures revealed that Thaumarchaeota contain a high diversity of membrane lipids that is related to phylogeny as well as growth characteristics. This analysis further revealed that all Thaumarchaeota contain the specific biomarkers crenarchaeol, methoxy archaeol, and saturated menaquinone-6

Unusual butane- and pentanetriol-based tetraether lipids in Methanomassiliicoccus luminyensis, a representative of the seventh order of methanogens

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 82 (2016): 4505-4516, doi:10.1128/AEM.00772-16.A new clade of archaea has recently been proposed to constitute the seventh methanogenic order, the Methanomassiliicoccales, which is related to the Thermoplasmatales and the uncultivated archaeal clades deep-sea hydrothermal vent Euryarchaeota group 2 and marine group II Euryarchaeota but only distantly related to other methanogens. In this study, we investigated the membrane lipid composition of Methanomassiliicoccus luminyensis, the sole cultured representative of this seventh order. The lipid inventory of M. luminyensis comprises a unique assemblage of novel lipids as well as lipids otherwise typical for thermophilic, methanogenic, or halophilic archaea. For instance, glycerol sesterpanyl-phytanyl diether core lipids found mainly in halophilic archaea were detected, and so were compounds bearing either heptose or methoxylated glycosidic head groups, neither of which have been reported so far for other archaea. The absence of quinones or methanophenazines is consistent with a biochemistry of methanogenesis different from that of the methanophenazine-containing methylotrophic methanogens. The most distinctive characteristic of the membrane lipid composition of M. luminyensis, however, is the presence of tetraether lipids in which one glycerol backbone is replaced by either butane- or pentanetriol, i.e., lipids recently discovered in marine sediments. Butanetriol dibiphytanyl glycerol tetraether (BDGT) constitutes the most abundant core lipid type (>50% relative abundance) in M. luminyensis. We have thus identified a source for these unusual orphan lipids. The complementary analysis of diverse marine sediment samples showed that BDGTs are widespread in anoxic layers, suggesting an environmental significance of Methanomassiliicoccales and/or related BDGT producers beyond gastrointestinal tracts.This study was funded by the European Research Council under the European Union's Seventh Framework Programme “Ideas” Specific Programme, ERC grant agreement no. 247153 (Advanced Grant DARCLIFE; principal investigator, K.-U.H.), and by the Deutsche Forschungsgemeinschaft through the Gottfried Wilhelm Leibniz Prize awarded to K.-U.H. (Hi 616-14-1) and instrument grant Inst 144/300-1 (LC-qToF system). A.S. and T.U. were financially supported by a UNI:DOCS fellowship and a short-term travel grant (KWA) from the University of Vienna (Austria).2016-11-1

Multiple environmental parameters impact lipid cyclization in Sulfolobus acidocaldarius

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/162708/2/emi15194.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/162708/1/emi15194_am.pd

CO_2-dependent carbon isotope fractionation in Archaea, Part I: Modeling the 3HP/4HB pathway

The 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) pathway of carbon fixation is found in thermophilic Crenarchaeota of the order Sulfolobales and in aerobic, ammonia-oxidizing Thaumarchaeota. Unlike all other known autotrophic carbon metabolisms, this pathway exclusively uses HCO_3- rather than CO_2 as the substrate for carbon fixation. Biomass produced by the 3HB/4HP pathway is relatively ^(13)C-enriched compared to biomass fixed by other autotrophic pathways, with total biosynthetic isotope effects (ε_(Ar)) of ca. 3‰ in the Sulfolobales and ca. 20‰ in the Thaumarchaeota. Explanations for the difference between these values usually invoke the dual effects of thermophily and growth at low pH (low [HCO_3-]) for the former group vs. mesophily and growth at pH > 7 (high [HCO_3-]) for the latter group. Here we examine the model taxa Metallosphaera sedula and Nitrosopumilus maritimususing an isotope flux-balance model to argue that the primary cause of different ε_(Ar) values more likely is the presence of carbonic anhydrase in M. sedula and its corresponding absence in N. maritimus. The results suggest that the pool of HCO_3-inside N. maritimus is out of isotopic equilibrium with CO_2 and that the organism imports < 10% HCO_3- from the extracellular environment. If correct and generalizable, the aerobic, ammonia-oxidizing marine Thaumarchaeota are dependent on passive CO_2 uptake and a slow rate of intracellular conversion to HCO_3-. Values of ε_(Ar) should therefore vary in response to growth rate (μ) and CO_2 availability, analogous to eukaryotic algae, but in the opposite direction: ε_(Ar) becomes smaller as [CO_(2(aq))] increases and/or μ decreases. Such an idea represents a testable hypothesis, both in the laboratory and in natural systems. Sensitivity to μ and CO_2 implies that measurements of ε_(Ar) may hold promise as a pCO_2 paleobarometer

Membrane lipid and expression responses of Saccharolobus islandicus REY15A to acid and cold stress

Archaea adjust the number of cyclopentane rings in their glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids as a homeostatic response to environmental stressors such as temperature, pH, and energy availability shifts. However, archaeal expression patterns that correspond with changes in GDGT composition are less understood. Here we characterize the acid and cold stress responses of the thermoacidophilic crenarchaeon Saccharolobus islandicus REY15A using growth rates, core GDGT lipid profiles, transcriptomics and proteomics. We show that both stressors result in impaired growth, lower average GDGT cyclization, and differences in gene and protein expression. Transcription data revealed differential expression of the GDGT ring synthase grsB in response to both acid stress and cold stress. Although the GDGT ring synthase encoded by grsB forms highly cyclized GDGTs with ≥5 ring moieties, S. islandicus grsB upregulation under acidic pH conditions did not correspond with increased abundances of highly cyclized GDGTs. Our observations highlight the inability to predict GDGT changes from transcription data alone. Broader analysis of transcriptomic data revealed that S. islandicus differentially expresses many of the same transcripts in response to both acid and cold stress. These included upregulation of several biosynthetic pathways and downregulation of oxidative phosphorylation and motility. Transcript responses specific to either of the two stressors tested here included upregulation of genes related to proton pumping and molecular turnover in acid stress conditions and upregulation of transposases in cold stress conditions. Overall, our study provides a comprehensive understanding of the GDGT modifications and differential expression characteristic of the acid stress and cold stress responses in S. islandicus

Report and preliminary results of R/V POSEIDON cruise POS539, Varna (Bulgaria) - Varna (Bulgaria) November 6 - November 21, 2019

The R/V POSEIDON cruise POS539 took place in the northwestern basin of the Black Sea (42°30’N to 44°N and 29°E to 31°E). The overarching aim of the campaign was to obtain sediment and water samples, including suspended particle material, from the various redox zones of the Black Sea. The campaign lasted between November 6th and November 21st 2019 and the collected samples were taken in order to investigate the activity and physiology of microorganisms involved in the conversion of nitrogen compounds and degradation of organic carbon under various oxygen conditions. The main topics of the cruise were: (a) to quantify the contribution of archaeal nitrifiers to the nitrogen and carbon cycles, b) to measure the production and consumption of the powerful greenhouse gases CH4 and N2O, c) to record palaeoenvironmental changes in high resolution, and d) to describe the complexity and identity of biopolymers. For this, water and sediment samples were retrieved from 10 discrete shelf and slope stations. First, ‘deep water’ transect was conducted, which included three stations with water depths over 2000 m. The second perpendicular transect encompassed stations that gradually transitioned from the deep parts of the slope towards the shelf (ca. 80 m depth). Additionally, two stations were setup north and south of the shelf transect, respectively, for paleoceanographic studies. Throughout the cruise the weather conditions were overwhelmingly good, only towards the end of the campaign gusty winds of 7 Bft were recorded. The recorded oceanographic conditions were in agreement with the expected water properties at all stations. Station activities were completed on November 20th at 14:00 local board time. On November 21st at 10:30 local time, R/V POSEIDON reached the port of Varna, Bulgaria, thus concluding the POS539 expedition. Analyses and results from the samples and experiments will provide a basis for our understanding of the microbial control on the carbon and nitrogen cycle of the Black Sea.13032

Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria.

Sediment-hosted CO2-rich aquifers deep below the Colorado Plateau (USA) contain a remarkable diversity of uncultivated microorganisms, including Candidate Phyla Radiation (CPR) bacteria that are putative symbionts unable to synthesize membrane lipids. The origin of organic carbon in these ecosystems is unknown and the source of CPR membrane lipids remains elusive. We collected cells from deep groundwater brought to the surface by eruptions of Crystal Geyser, sequenced the community, and analyzed the whole community lipidome over time. Characteristic stable carbon isotopic compositions of microbial lipids suggest that bacterial and archaeal CO2 fixation ongoing in the deep subsurface provides organic carbon for the complex communities that reside there. Coupled lipidomic-metagenomic analysis indicates that CPR bacteria lack complete lipid biosynthesis pathways but still possess regular lipid membranes. These lipids may therefore originate from other community members, which also adapt to high in situ pressure by increasing fatty acid unsaturation. An unusually high abundance of lysolipids attributed to CPR bacteria may represent an adaptation to membrane curvature stress induced by their small cell sizes. Our findings provide new insights into the carbon cycle in the deep subsurface and suggest the redistribution of lipids into putative symbionts within this community

From ether to acid: a plausible degradation pathway of glycerol dialkyl glycerol tetraethers

Glycerol dialkyl glycerol tetraethers (GDGTs) are ubiquitous microbial lipids with extensive demonstrated and potential roles as paleoenvironmental proxies. Despite the great attention they receive, comparatively little is known regarding their diagenetic fate. Putative degradation products of GDGTs, identified as hydroxyl and carboxyl derivatives, were detected in lipid extracts of marine sediment, seep carbonate, hot spring sediment and cells of the marine thaumarchaeon Nitrosopumilus maritimus. The distribution of GDGT degradation products in environmental samples suggests that both biotic and abiotic processes act as sinks for GDGTs. More than a hundred newly recognized degradation products afford a view of the stepwise degradation of GDGT via (1) ether bond hydrolysis yielding hydroxyl isoprenoids, namely, GDGTol (glycerol dialkyl glycerol triether alcohol), GMGD (glycerol monobiphytanyl glycerol diether), GDD (glycerol dibiphytanol diether), GMM (glycerol monobiphytanol monoether) and bpdiol (biphytanic diol); (2) oxidation of isoprenoidal alcohols into corresponding carboxyl derivatives and (3) chain shortening to yield C39and smaller isoprenoids. This plausible GDGT degradation pathway from glycerol ethers to isoprenoidal fatty acids provides the link to commonly detected head-to-head linked long chain isoprenoidal hydrocarbons in petroleum and sediment samples. The problematic C80to C82tetraacids that cause naphthenate deposits in some oil production facilities can be generated from H-shaped glycerol monoalkyl glycerol tetraethers (GMGTs) following the same process, as indicated by the distribution of related derivatives in hydrothermally influenced sediments.Seventh Framework Programme (European Commission) (ERC Grant 247153

Einflüsse auf die Lipidzusammensetzung mariner planktonischer Thaumarchaeen

Marine ammonia-oxidizing archaea of the phylum Thaumarchaeota synthesize glycerol dibiphytanyl glycerol tetraether (GDGT) membrane lipids that are used as for the reconstruction of sea surface temperatures by means of the TEX86 paleothermometer. Discrepancies between observed and predicted TEX86-temperatures throughout the global ocean indicate that the physiological and ecological controls on lipid composition in planktonic Thaumarchaeota remain poorly understood. In this thesis, the influence of growth phase, temperature, pH, and salinity on the membrane lipid composition of Thaumarchaeota were investigated. The results indicate that TEX86 is not only influenced by temperature but similarly by growth phase and community composition, which compromises its utility as a paleothermometer. A comprehensive study of the lipidomes of 11 thaumarchaeal cultures revealed that Thaumarchaeota contain a high diversity of membrane lipids that is related to phylogeny as well as growth characteristics. This analysis further revealed that all Thaumarchaeota contain the specific biomarkers crenarchaeol, methoxy archaeol, and saturated menaquinone-6