We conducted a survey of archaeal GDGT (glycerol dibiphytanyl glycerol tetraether) distributions in marine sediments deposited in a range of depositional settings. The focus was comparison of two ...pools presumed to have distinct geobiological significance, i.e. intact polar GDGTs (IP GDGTs) and core GDGTs (C GDGTs). The former pool has been suggested to be related to living communities of benthic archaea in marine sediments, while the latter is commonly interpreted to consist of molecular fossils from past planktonic archaeal communities that inhabited the surface ocean. Understanding the link between these two pools is important for assessment of the validity of current molecular proxies for sedimentary archaeal biomass and past sea surface temperatures. The relative distributions of GDGTs in the two pools in a core at a CH
4 rich site in the Black Sea provide evidence for in situ production of glycosidic IP GDGTs and their subsequent degradation to corresponding C GDGTs on timescales that are short in geological terms. In addition, we monitored the relationship between the IP GDGT and C GDGT pools in a sample set from various ocean basins with subseafloor depth from a few cm to 320
m and 0 to 4
Myr in age. Notable differences between the two pools can be summarized as follows: the GDGT with acyclic biphytanes, GDGT-0, and its analogues with two and three cyclopentane moieties (GDGT-2 and -3) are generally more abundant in the pool of IP GDGTs, while crenarchaeol tends to be more abundant in the C GDGT pool. Consequently, the ring index is generally higher for the C GDGTs while TEX
86, a molecular proxy ratio not considering the two major GDGTs, tends to be higher in the IP GDGT pool. These differences in the proportion of individual GDGTs in the two pools are probably due to in situ production of IP GDGTs with distributions differing from those of C GDGTs. Despite these differences, we observed significant correlation of these two ratios between the two pools. Specifically, in both pools TEX
86 is high in sediments from warm oceanic regimes and low in cold regimes. We discuss these relationships and suggest that recycling of core GDGTs by benthic archaea is an important mechanism linking both molecular pools.
Significance Lipid biomarkers in geological samples are important informants regarding past environments and ecosystems. Conventional biomarker analysis is labor intensive and requires relatively ...large sediment or rock samples; temporal resolution is consequently low. Here, we present an approach that has the potential to revolutionize paleoenvironmental biomarker research; it avoids wet-chemical sample preparation and enables analysis of biomarkers directly on sediment cores at submillimeter spatial resolution. Our initial application to a sediment core deposited during the Holocene climate optimum in the Mediterranean Sea reveals a new view of how small-scale variations in lipid distribution are integrated into commonly reported signals obtained by conventional analysis and demonstrates a strong influence of the ∼200-y de Vries solar cycle on sea-surface temperatures and planktonic archaeal ecology.
Marine microorganisms adapt to their habitat by structural modification of their membrane lipids. This concept is the basis of numerous molecular proxies used for paleoenvironmental reconstruction. Archaeal tetraether lipids from ubiquitous marine planktonic archaea are particularly abundant, well preserved in the sedimentary record and used in several molecular proxies. We here introduce the direct, extraction-free analysis of these compounds in intact sediment core sections using laser desorption ionization (LDI) coupled to Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS). LDI FTICR-MS can detect the target lipids in single submillimeter-sized spots on sediment sections, equivalent to a sample mass in the nanogram range, and could thus pave the way for biomarker-based reconstruction of past environments and ecosystems at subannual to decadal resolution. We demonstrate that ratios of selected archaeal tetraethers acquired by LDI FTICR-MS are highly correlated with values obtained by conventional liquid chromatography/MS protocols. The ratio of the major archaeal lipids, caldarchaeol and crenarchaeol, analyzed in a 6.2-cm intact section of Mediterranean sapropel S1 at 250-µm resolution (∼4-y temporal resolution), provides an unprecedented view of the fine-scale patchiness of sedimentary biomarker distributions and the processes involved in proxy signal formation. Temporal variations of this lipid ratio indicate a strong influence of the ∼200-y de Vries solar cycle on reconstructed sea surface temperatures with possible amplitudes of several degrees, and suggest signal amplification by a complex interplay of ecological and environmental factors. Laser-based biomarker analysis of geological samples has the potential to revolutionize molecular stratigraphic studies of paleoenvironments.
The subsurface realm is colonized by microbial communities to depths of >1000 meters below the seafloor (m.b.sf.), but little is known about overall diversity and microbial distribution patterns at ...the most profound depths. Here we show that not only Bacteria and Archaea but also Eukarya occur at record depths in the subseafloor of the Canterbury Basin. Shifts in microbial community composition along a core of nearly 2 km reflect vertical taxa zonation influenced by sediment depth. Representatives of some microbial taxa were also cultivated using methods mimicking in situ conditions. These results suggest that diverse microorganisms persist down to 1922 m.b.sf. in the seafloor of the Canterbury Basin and extend the previously known depth limits of microbial evidence (i) from 159 to 1740 m.b.sf. for Eukarya and (ii) from 518 to 1922 m.b.sf. for Bacteria.
Ammonia-oxidizing archaea (AOA) are abundant and widely distributed microorganisms in aquatic and terrestrial habitats. By catalyzing the first and rate limiting step in nitrification, these ...chemolithoautotrophs play a significant role in the global nitrogen cycle and contribute to primary production. Here, the carbon isotopic fractionation relative to inorganic carbon source was determined for bulk biomass, biphytanes and polar lipid bound sugars of a marine AOA pure culture. Bulk biomass and biphytanes from Nitrosopumilus maritimus showed identical carbon isotope fractionation (εDIC/bulk and εDIC/byphytanes) of ca. −20‰. The glycoside head groups were mainly glucose, mannose and inositol, and exhibited different carbon isotopic composition. In general, these monosaccharides were enriched in 13C (ε −6.1‰ to −13.8‰) relative to bulk biomass and biphytanes. The fact that the carbon isotope composition of the biphytanes reflected that of the bulk biomass of N. maritimus suggests that the depletion of 13C in both biomass and biphytanes resulted mainly from the carbon isotope discrimination by the bicarbonate-fixing enzyme in the autotrophic hydroxypropionate/hydroxybutyrate cycle. Our results further revealed that lipid compounds represent suitable biomarkers for determining δ13C values of archaeal ammonia oxidizers without biosynthetic correction.
Archaea play an important role in marine biogeochemical cycle; however, their phylogenetic distribution and lipid composition in the hadal zone (6–11 km water depth) are poorly known. Here, we ...analyzed archaeal membrane lipids and 16S rRNA gene sequences in sediments from Mariana Trench (MT), Massau Trench (MS), and New Britain Trench (NBT), varying from 1,560 to 10,840 m depth. Forty‐two intact polar lipids (IPLs) were identified, including glycerol dialkyl glycerol tetraethers (GDGTs), OH‐GDGTs, glycerol dialkyl diethers (GDDs), and archaeol (AR) with polar headgroups of monohexose (1G), dihexose (2G), trihexose (3G), and hexose‐phosphohexose (HPH). Compositional and spatial distribution patterns of archaeal lipids suggest benthic Thaumarchaeota as a major source for IPLs, consistent with the predominance of Thaumarchaeota genes (>80%). The redundancy analysis (RDA) based on lipid and 16S rRNA data separates samples into three groups: extremely deep water (MT), significant terrestrial influence (NBT 1, 4, and 6), and predominant marine influence (MS, NBT 2, 3, 7, and 10). 1G‐GDDs and 1G‐AR positively correlate with water depth, likely reflecting the adaptation of benthic archaea to elevated hydrostatic pressure or variation of archaeal community in trench sediments. Bathyarchaeota are more abundant in sediments receiving terrestrial input; this pattern was attributed to their capability of utilizing terrestrial organic matter as an energy source. Our study highlights important environmental influences (e.g., pressure and organic matter quality and quantity) on benthic archaeal community and archaeal IPL compositions, which should be considered when IPLs and core lipids are applied as chemotaxonomic markers and paleo‐proxies.
Key Points
Benthic archaea are a major source for IPLs in trench sediments
Some IPLs positively correlate with water depth, reflecting adaption of archaea to hydrostatic pressure or changes of archaeal community
Bathyarchaeota are more abundant in sediments receiving terrestrial input, attributed to utilization of terrestrial organic matter
Plain Language Summary
This work is the first report on intact polar lipids (IPLs) of archaea in the hadal trenches, the deepest ocean realm with water depth exceeding 6,000 m. We have investigated in IPL biomarker 16S rRNA gene sequences and biogeochemical parameters in 19 sediments from the Mariana Trench, Massau Trench, and New Britain Trench. These samples are characterized by different water depth (1,560 to 10,840 m), net primary productivity (48 to 123 C m−2 year−1), and terrestrial influence. By comparing biomarker, gene data, and bulk geochemical parameters, we have achieved three key findings: (1) Benthic Thaumarchaeota are a major source for IPLs in hadal sediments; (2) Some IPLs positively correlate with water depth, likely reflecting an adaption mechanism of benthic archaea to elevated hydrostatic pressure or variation of archaeal community in different environments; and (3) Bathyarchaeota are more abundant in sediments receiving terrestrial input (New Britain Trench); this pattern is attributed to their capability of utilizing terrestrial organic matter as an energy source. Our findings provide important information toward understanding of the distribution and adaptation of hadal microbes to extremely high pressure, dark, and food‐depleted environments.
Hydroxylated glycerol dialkyl glycerol tetraethers (hydroxy-GDGTs) were detected in marine sediments of diverse depositional regimes and ages. Mass spectrometric evidence, complemented by information ...gleaned from two-dimensional (2D) 1H–13C nuclear magnetic resonance (NMR) spectroscopy on minute quantities of target analyte isolated from marine sediment, allowed us to identify one major compound as a monohydroxy-GDGT with acyclic biphytanyl moieties (OH-GDGT-0). NMR spectroscopic and mass spectrometric data indicate the presence of a tertiary hydroxyl group suggesting the compounds are the tetraether analogues of the widespread hydroxylated archaeol derivatives that have received great attention in geochemical studies of the last two decades. Three other related compounds were assigned as acyclic dihydroxy-GDGT (2OH-GDGT-0) and monohydroxy-GDGT with one (OH-GDGT-1) and two cyclopentane rings (OH-GDGT-2). Based on the identification of hydroxy-GDGT core lipids, a group of previously reported unknown intact polar lipids (IPLs), including the ubiquitously distributed H341-GDGT (Lipp J. S. and Hinrichs K. -U. (2009) Structural diversity and fate of intact polar lipids in marine sediments. Geochim. Cosmochim. Acta 73, 6816–6833), and its analogues were tentatively identified as glycosidic hydroxy-GDGTs. In addition to marine sediments, we also detected hydroxy-GDGTs in a culture of Methanothermococcus thermolithotrophicus. Given the previous finding of the putative polar precursor H341-GDGT in the planktonic marine crenarchaeon Nitrosopumilus maritimus, these compounds are synthesized by representatives of both cren- and euryarchaeota. The ubiquitous distribution and apparent substantial abundance of hydroxy-GDGT core lipids in marine sediments (up to 8% of total isoprenoid core GDGTs) point to their potential as proxies.
Archaeal membrane lipids known as glycerol dibiphytanyl glycerol tetraethers (GDGTs) are the basis of the TEX86 paleotemperature proxy. Because GDGTs preserved in marine sediments are thought to ...originate mainly from planktonic, ammonia-oxidizing Thaumarchaeota, the basis of the correlation between TEX86 and sea surface temperature (SST) remains unresolved: How does TEX86 predict surface temperatures, when maximum thaumarchaeal activity occurs below the surface mixed layer and TEX86 does not covary with in situ growth temperatures? Here we used isothermal studies of the model thaumarchaeon Nitrosopumilus maritimus SCM1 to investigate how GDGT composition changes in response to ammonia oxidation rate. We used continuous culture methods to avoid potential confounding variables that can be associated with experiments in batch cultures. The results show that the ring index scales inversely (R² = 0.82) with ammonia oxidation rate (ϕ), indicating that GDGT cyclization depends on available reducing power. Correspondingly, the TEX86 ratio decreases by an equivalent of 5.4 °C of calculated temperature over a 5.5 fmol·cell−1·d−1 increase in ϕ. This finding reconciles other recent experiments that have identified growth stage and oxygen availability as variables affecting TEX86. Depth profiles from the marine water column show minimum TEX86 values at the depth of maximum nitrification rates, consistent with our chemostat results. Our findings suggest that the TEX86 signal exported from the water column is influenced by the dynamics of ammonia oxidation. Thus, the global TEX86–SST calibration potentially represents a composite of regional correlations based on nutrient dynamics and global correlations based on archaeal community composition and temperature.
Abstract
Correction to: The ISME Journal (2014) 8, 1370–1380; doi:10.1038/ismej.2013.250; published online 16 January 2014 Since the publication of this article, it has come to the authors’ attention ...that the study accession number deposited in the Sequence Read Archive was omitted from the article. The study accession number is ERP002102.
The hydrothermal sediments of Guaymas Basin, an active spreading center in the Gulf of California (Mexico), are rich in porewater methane, short-chain alkanes, sulfate and sulfide, and provide a ...model system to explore habitat preferences of microorganisms, including sulfate-dependent, methane- and short chain alkane-oxidizing microbial communities. In this study, hot sediments (above 60°C) covered with sulfur-oxidizing microbial mats surrounding a hydrothermal mound (termed "Mat Mound") were characterized by porewater geochemistry of methane, C2-C6 short-chain alkanes, sulfate, sulfide, sulfate reduction rate measurements, in situ temperature gradients, bacterial and archaeal 16S rRNA gene clone libraries and V6 tag pyrosequencing. The most abundantly detected groups in the Mat mound sediments include anaerobic methane-oxidizing archaea of the ANME-1 lineage and its sister clade ANME-1Guaymas, the uncultured bacterial groups SEEP-SRB2 within the Deltaproteobacteria and the separately branching HotSeep-1 Group; these uncultured bacteria are candidates for sulfate-reducing alkane oxidation and for sulfate-reducing syntrophy with ANME archaea. The archaeal dataset indicates distinct habitat preferences for ANME-1, ANME-1-Guaymas, and ANME-2 archaea in Guaymas Basin hydrothermal sediments. The bacterial groups SEEP-SRB2 and HotSeep-1 co-occur with ANME-1 and ANME-1Guaymas in hydrothermally active sediments underneath microbial mats in Guaymas Basin. We propose the working hypothesis that this mixed bacterial and archaeal community catalyzes the oxidation of both methane and short-chain alkanes, and constitutes a microbial community signature that is characteristic for hydrothermal and/or cold seep sediments containing both substrates.
Significance
The membrane lipids of marine Archaea form the basis of the temperature proxy called TEX
86
, which is used for paleoclimate reconstructions from the Jurassic to the present. To date ...there remains no satisfactory explanation for how planktonic Archaea are able to record water column temperatures, because TEX
86
does not correlate well with in situ growth temperatures in the modern ocean. Here we show that the TEX
86
lipid ratio changes in response to cellular growth rate, which is controlled by the ammonia oxidation rate. This implies that variation in the TEX
86
ratio with water depth is influenced by the metabolic activity of Thaumarchaeota in the water column.
Archaeal membrane lipids known as glycerol dibiphytanyl glycerol tetraethers (GDGTs) are the basis of the TEX
86
paleotemperature proxy. Because GDGTs preserved in marine sediments are thought to originate mainly from planktonic, ammonia-oxidizing Thaumarchaeota, the basis of the correlation between TEX
86
and sea surface temperature (SST) remains unresolved: How does TEX
86
predict surface temperatures, when maximum thaumarchaeal activity occurs below the surface mixed layer and TEX
86
does not covary with in situ growth temperatures? Here we used isothermal studies of the model thaumarchaeon
Nitrosopumilus maritimus
SCM1 to investigate how GDGT composition changes in response to ammonia oxidation rate. We used continuous culture methods to avoid potential confounding variables that can be associated with experiments in batch cultures. The results show that the ring index scales inversely (
R
2
= 0.82) with ammonia oxidation rate (ϕ), indicating that GDGT cyclization depends on available reducing power. Correspondingly, the TEX
86
ratio decreases by an equivalent of 5.4 °C of calculated temperature over a 5.5 fmol·cell
−1
·d
−1
increase in ϕ. This finding reconciles other recent experiments that have identified growth stage and oxygen availability as variables affecting TEX
86
. Depth profiles from the marine water column show minimum TEX
86
values at the depth of maximum nitrification rates, consistent with our chemostat results. Our findings suggest that the TEX
86
signal exported from the water column is influenced by the dynamics of ammonia oxidation. Thus, the global TEX
86
–SST calibration potentially represents a composite of regional correlations based on nutrient dynamics and global correlations based on archaeal community composition and temperature.
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