Rewetting the hyper-arid Atacama Desert soil reactivates a carbon-starved microbial decomposer community and also triggers archaeal metabolism.

Extreme environmental conditions make soils of the hyper-arid Atacama Desert one of the most hostile habitats for life on the planet. During the short intervals of moisture availability that occur, it remains unresolved how soil microorganisms physiologically respond to such dramatic environmental changes. Therefore, we simulated a precipitation event - without (H2O) and with (H2O + C) labile carbon (C) supplementation - and investigated the responses in microbial communities (using phospholipid fatty acids (PLFAs) and archaeal glycerol dialkyl glycerol tetraether (GDGTs)) and physiology (by means of respiration, bacterial and fungal growth and C-use efficiency (CUE)) during a five-day incubation. We demonstrated that bacterial and fungal growth does occur in these extreme soils following rewetting, albeit at 100-10,000-fold lower rates compared to previously studied soil systems. C supplementation increased levels of bacterial growth and respiration responses by 5- and 50-fold, respectively, demonstrating a C-limited microbial decomposer community. While the microbial CUE following rewetting was c. 14 %, the addition of labile C during rewetting resulted in a substantial reduction (c. 1.6 %). Consistent with these interpretations, the PLFA composition clearly shifted from saturated towards more unsaturated and branched PLFAs, which could arise from (i) a physiological adaptation of the cell membrane to changing osmotic conditions or (ii) a community composition shift. Significant increases in total PLFA concentrations were solely found with H2O + C addition. Contrary to other recent studies, we found evidence for a metabolically active archaeal community in these hyper-arid soils upon rewetting. We conclude that (i) microorganisms in this extreme soil habitat can be activated and grow within days following rewetting, (ii) available C is the limiting factor for microbial growth and biomass gains, and (iii) that an optimization of tolerating the extreme conditions while maintaining a high CUE comes at the expense of very poor resource-use efficiency during high resource availability.

Microbial methane cycling in sediments of Arctic thermokarst lagoons.

Thermokarst lagoons represent the transition state from a freshwater lacustrine to a marine environment, and receive little attention regarding their role for greenhouse gas production and release in Arctic permafrost landscapes. We studied the fate of methane (CH4 ) in sediments of a thermokarst lagoon in comparison to two thermokarst lakes on the Bykovsky Peninsula in northeastern Siberia through the analysis of sediment CH4 concentrations and isotopic signature, methane-cycling microbial taxa, sediment geochemistry, lipid biomarkers, and network analysis. We assessed how differences in geochemistry between thermokarst lakes and thermokarst lagoons, caused by the infiltration of sulfate-rich marine water, altered the microbial methane-cycling community. Anaerobic sulfate-reducing ANME-2a/2b methanotrophs dominated the sulfate-rich sediments of the lagoon despite its known seasonal alternation between brackish and freshwater inflow and low sulfate concentrations compared to the usual marine ANME habitat. Non-competitive methylotrophic methanogens dominated the methanogenic community of the lakes and the lagoon, independent of differences in porewater chemistry and depth. This potentially contributed to the high CH4 concentrations observed in all sulfate-poor sediments. CH4 concentrations in the freshwater-influenced sediments averaged 1.34 ± 0.98 µmol g-1 , with highly depleted δ13 C-CH4 values ranging from -89‰ to -70‰. In contrast, the sulfate-affected upper 300 cm of the lagoon exhibited low average CH4 concentrations of 0.011 ± 0.005 µmol g-1 with comparatively enriched δ13 C-CH4 values of -54‰ to -37‰ pointing to substantial methane oxidation. Our study shows that lagoon formation specifically supports methane oxidizers and methane oxidation through changes in pore water chemistry, especially sulfate, while methanogens are similar to lake conditions.

Biosignatures in chimney structures and sediment from the Loki's Castle low-temperature hydrothermal vent field at the Arctic Mid-Ocean Ridge.

We investigated microbial life preserved in a hydrothermally inactive silica­barite chimney in comparison with an active barite chimney and sediment from the Loki's Castle low-temperature venting area at the Arctic Mid-Ocean Ridge (AMOR) using lipid biomarkers. Carbon and sulfur isotopes were used to constrain possible metabolic pathways. Multiple sulfur (dδ34S, Δ33S) isotopes on barite over a cross section of the extinct chimney range between 21.1 and 22.5 % in δ34S, and between 0.020 and 0.034 % in Δ33S, indicating direct precipitation from seawater. Biomarker distributions within two discrete zones of this silica­barite chimney indicate a considerable difference in abundance and diversity of microorganisms from the chimney exterior to the interior. Lipids in the active and inactive chimney barite and sediment were dominated by a range of 13C-depleted unsaturated and branched fatty acids with δ13C values between -39.7 and -26.7 %, indicating the presence of sulfur-oxidizing and sulfate-reducing bacteria. The majority of lipids (99.5 %) in the extinct chimney interior that experienced high temperatures were of archaeal origin. Unusual glycerol monoalkyl glycerol tetraethers (GMGT) with 0­4 rings were the dominant compounds suggesting the presence of mainly (hyper-) thermophilic archaea. Isoprenoid hydrocarbons with δ13C values as low as -46 % also indicated the presence of methanogens and possibly methanotrophs.

A multi-proxy study of anaerobic ammonium oxidation in marine sediments of the Gullmar Fjord, Sweden.

Anaerobic ammonium oxidation (anammox) is an important process for nitrogen removal in marine pelagic and benthic environments and represents a major sink in the global nitrogen cycle. We applied a suite of complementary methods for the detection and enumeration of anammox activity and anammox bacteria in marine sediments of the Gullmar Fjord, and compared the results obtained with each technique. (15) N labelling experiments showed that nitrogen removal through N2 production was essentially limited to the upper 2 cm of the sediment, where anammox contributed 23-47% of the total production. The presence of marine anammox bacteria belonging to the genus 'Candidatus Scalindua' was shown by 16S rRNA gene sequence comparison. FISH counts of anammox bacteria correlated well with anammox activity, while quantitative PCR may have underestimated the number of anammox bacterial 16S rRNA gene copies at this site. Potential nitrogen conversion by anammox ranged from 0.6 to 4.8 fmol N cell(-1) day(-1) , in agreement with previous measurements in the marine environment and in bioreactors. Finally, intact ladderane glycerophospholipid concentrations better reflected anammox activity and abundance than ladderane core lipid concentrations, most likely because the core lipid fraction contained a substantial fossil component, especially deeper in the sediment.

Impact of temperature on ladderane lipid distribution in anammox bacteria.

Anaerobic ammonium-oxidizing (anammox) bacteria have the unique ability to synthesize fatty acids containing linearly concatenated cyclobutane rings, termed "ladderane lipids." In this study we investigated the effect of temperature on the ladderane lipid composition and distribution in anammox enrichment cultures, marine particulate organic matter, and surface sediments. Under controlled laboratory conditions we observed an increase in the amount of C(20) [5]-ladderane fatty acids compared with the amount of C(18) [5]-ladderane fatty acids with increasing temperature and also an increase in the amount of C(18) [5]-ladderane fatty acids compared with the amount of C(20) [5]-ladderane fatty acids with decreasing temperature. Combining these data with results from the natural environment showed a significant (R(2) = 0.85, P = <0.0001, n = 121) positive sigmoidal relationship between the amounts of C(18) and C(20) [5]-ladderane fatty acids and the in situ temperature; i.e., there is an increase in the relative abundance of C(18) [5]-ladderane fatty acids at lower temperatures and vice versa, particularly at temperatures between 12 degrees C and 20 degrees C. Novel shorter (C(16)) and longer (C(22) to C(24)) ladderane fatty acids were also identified, but their relative amounts were small and did not change with temperature. The adaptation of ladderane fatty acid chain length to temperature changes is similar to the regulation of common fatty acid composition in other bacteria and may be the result of maintaining constant membrane fluidity under different temperature regimens (homeoviscous adaptation). Our results can potentially be used to discriminate between the origins of ladderane lipids in marine sediments, i.e., to determine if ladderanes are produced in situ in relatively cold surface sediments or if they are fossil remnants originating from the warmer upper water column.

16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs.

Anammox, the oxidation of ammonium with nitrite to dinitrogen gas under anoxic conditions, is an important process in mesophilic environments such as wastewaters, oceans and freshwater systems, but little is known of this process at elevated temperatures. In this study, we investigated anammox in microbial mats and sediments obtained from several hot springs in California and Nevada, using geochemical and molecular microbiological methods. Anammox bacteria-specific ladderane core lipids with concentrations ranging between 0.3 and 52 ng g(-1) sediment were detected in five hot springs analyzed with temperatures up to 65 degrees C. In addition, 16S rRNA gene analysis showed the presence of genes phylogenetically related to the known anammox bacteria Candidatus Brocadia fulgida, Candidatus Brocadia anammoxidans and Candidatus Kuenenia stuttgartiensis (96.5-99.8% sequence identity) in three hot springs with temperatures up to 52 degrees C. Our data indicate that anammox bacteria may be able to thrive at thermophilic temperatures and thus may play a significant role in the nitrogen cycle of hot spring environments.

Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents.

Recent studies indicate that ammonia is an important electron donor for the oxidation of fixed nitrogen, both in the marine water column and sediments. This process, known as anammox, has so far only been observed in a large range of temperature habitats. The present study investigated the role of anammox in hydrothermal settings. During three oceanographic expeditions to the Mid-Atlantic Ridge, hydrothermal samples were collected from five vent sites, at depths ranging from 750 to 3650 m from cold to hot habitats. Evidence for the occurrence of anammox in these particular habitats was demonstrated by concurrent surveys, including the amplification of 16S rRNA gene sequences related to known anammox bacteria, ladderanes lipids analysis and measurement of a (14)N(15)N dinitrogen production in isotope-pairing experiments at 60 and 85 degrees C. Together these results indicate that new deep-branching anammox bacteria may be active in these hot habitats.

Improved analysis of ladderane lipids in biomass and sediments using high-performance liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry.

Ladderane lipids, containing three or five linearly concatenated cyclobutane moieties, are considered to be unique biomarkers for the process of anaerobic ammonium oxidation, an important link in the oceanic nitrogen cycle. Due to the thermal lability of the strained cyclobutane moieties, the ladderane lipids are difficult to analyze by gas chromatography. A method combining high-performance liquid chromatography coupled to positive ion atmospheric pressure chemical ionization tandem mass spectrometry (HPLC/APCI-MS/MS) was developed for the analysis of the most abundant ladderane lipids, occurring as fatty acids and ether-bound to glycerol. Detection was achieved by selective reaction monitoring of four specific fragmentations per ladderane lipid. Detection limits of 30-35 pg injected on-column and a linear response (r(2) > 0.99) over nearly 3 orders of magnitude were achieved for all compounds. Using this method, these unique ladderane lipids were for the first time identified in a surface sediment from the Gullmarsfjorden, in concentrations ranging from 1.1-5.5 ng/g for the ladderane fatty acids and of 0.7 ng/g for the monoether. It is foreseen that this method will allow the investigation of the occurrence of anaerobic ammonium oxidation in natural settings in much greater detail than before.