Effects of temperature and pH on archaeal membrane lipid distributions in freshwater wetlands
Introduction
Wetland sediments are unique terrestrial archives that can provide insights into climatic and environmental change on land on both recent and geological timescales (Barber, 1993, Pancost et al., 2007, Huguet et al., 2010, Coffinet et al., 2015, Coffinet et al., 2018, Zheng et al., 2015, Naafs et al., 2018b, Inglis et al., 2019). They are also key components of the global carbon cycle, being the largest natural source of CH4 to the atmosphere, a greenhouse gas with 25 times the warming potential of CO2 on a centennial time-scale (Tian et al., 2015). In response to rising global temperatures, wetland CH4 emissions are projected to increase by 33–60% by 2100 (Collins et al., 2013, Wania et al., 2013, Dean et al., 2018), acting as a positive feedback to anthropogenic climate change. Such methane emissions are ultimately driven by diverse archaeal assemblages with key roles in the processing of organic matter, notably mediating methanogenesis and the anaerobic oxidation of methane (AOM) (Cadillo-Quiroz et al., 2006, Zhu et al., 2012, Andersen et al., 2013, Bridgham et al., 2013, Segarra etal., 2015, Valenzuela et al., 2017).
Wetland environments preserve diverse archaeal lipid assemblages (Pancost and Sinninghe Damsté, 2003, Pancost et al., 2003, Weijers et al., 2004, Zheng et al., 2011, Naafs et al., 2018b, Naafs et al., 2019, Yang et al., 2018) that have the potential to inform studies of archaeal-mediated carbon cycle-climate dynamics, both in modern and ancient settings and/or to be used as palaeoclimatic markers. In recent years an increasingly diverse suite of archaeal core tetraether structures has been identified in environmental samples (including peat) (Liu et al., 2012, Liu et al., 2016, Naafs et al., 2018a) and cultures (Bauersachs et al., 2015, Becker et al., 2016), increasing the potential of lipid-focused chemotaxonomic and/or functional microbial studies and opening up novel avenues for proxy development. With a few notable exceptions (Weijers et al., 2004, Naafs et al., 2018b, Naafs et al., 2018a, Yang et al., 2018), many of these compounds remain poorly characterised in wetland environments. Despite this, and unlike in other environments, such as the open ocean (Schouten et al., 2002, Schouten et al., 2013), the main environmental and ecological drivers of archaeal membrane lipid composition in wetlands - particularly with regards to core lipid types such as isoGDGT isomers and Me-GDGTs - are relatively poorly constrained. This contributes to an overall incomplete understanding of archaeal ecology and carbon cycling in wetlands, particularly in tropical regions, and of the complex relationships of such microbial communities with climate and environmental change. In addition, it limits the interpretation of potentially informative lipid signatures in ancient sediments and other mesophilic settings.
The aims of this study were to examine the composition of archaeal lipids in three different types of modern wetlands, and to explore the ecological and environmental factors that drive differences in their distribution. We focused not only on the more widely studied isoGDGTs (De Rosa and Gambacorta, 1988, Schouten et al., 2013) and their chromatographically distinct earlier eluting isomers (Becker et al., 2013, Hopmans et al., 2016, Liu et al., 2016), but also examined the broader archaeal tetraether lipid distribution (Fig. S1 shows the lipid structures), in our three main study sites. This includes: i) butane-/pentane- dibiphytanyl glycerol tetraethers (B-/PDGTs) that have butanetriol or pentanetriol backbones instead of one of the more common glycerol moieties (Zhu et al., 2014, Becker et al., 2016); ii) methyl-GDGTs (Me-GDGTs) that incorporate up to three additional methyl groups on their biphytanyl chain (Knappy et al., 2015), and iii) Me-GMGTs, which incorporate an extra methyl group on the biphytanyl chain, as well as the covalent cross-link found in regular isoGMGTs (Knappy et al., 2014). GMGTs are a lipid class that were recently found to be abundant in some peats (Naafs et al., 2018a). We characterised both core lipids and the acid-hydrolysed core lipid derivatives of intact polar lipids (IPL-derived core lipids). IPLs are commonly used as markers for in situ, live, microbial cells in the environment, due to their relatively rapid degradation following cell lysis (White et al., 1979, Harvey et al., 1986, Lipp et al., 2008), although it has also been shown that they can be preserved over longer time-scales in some settings (Bauersachs et al., 2010, Logemann et al., 2011, Lengger et al., 2013, Lengger et al., 2014, Xie et al., 2013). We focused in detail on three wetland sites: Sebangau (Indonesia), the Florida Everglades (USA) and Tor Royal, Dartmoor (UK). These three sites constitute distinct wetland types with differing physicochemical and environmental characteristics. In addition, two of these sites are tropical wetland regions (i.e. the Florida Everglades and Sebangau, Indonesia), which are poorly studied ecosystem types in terms of lipid geochemistry. As well as these three sites, we examined the composition of certain archaeal lipids (isoGDGT-0-4, their isomers and crenarchaeol) in a globally distributed set of wetlands (Naafs et al., 2017), allowing for the identification and illustration of global patterns in archaeal lipid distributions. Collectively, this study provides insights into the environmental controls on archaeal lipid membrane regulation in mesophilic settings such as wetlands and provides context for future studies utilising archaeal lipids to elucidate biogeochemical processes in modern and ancient wetlands.
Section snippets
Sites and sampling
We focused primarily on three wetland sites. These were: Sebangau (Indonesia), Everglades (USA), and Tor Royal (UK). Site details are summarised in Table 1 (with additional details in Table S1). For each site, one core was analysed, though we recognise that wetlands are spatially heterogenous environments and therefore each core can only be considered partially representative of a particular wetland site.
Occurrence and depth variation of CL and IPL archaeal lipids within three primary wetland sites
The relative abundance of individual compounds and classes varied both between and within the three sites. Whilst we characterised both IPL-derived and core lipids, the depth profiles of both lipid groups were similar, except where noted, and are therefore largely referred to collectively.
Lipids detected at our sites included characteristic archaeal membrane lipids such as the isoGDGTs, in particular isoGDGT-0, which despite varying in relative abundance among sites was generally the dominant
Discussion
The relatively low taxonomic specificity of most archaeal lipids (de Rosa et al., 1986, Schouten et al., 2013, Bauersachs et al., 2015, Elling et al., 2017) makes it challenging to directly assign specific sources to compounds in environmental samples. This is made more challenging by the high diversity of archaeal communities in wetlands (Cadillo-Quiroz et al., 2008, Narrowe et al., 2017) and the likelihood of a significant input from uncultured phyla for which lipid compositions are not
Conclusions
We determined the relative abundances of diverse archaeal lipid types in three wetland study sites, and further contextualised these, where possible, with a re-analysis of a global database of archaeal lipids in wetlands. The latter broadly confirms that findings based on our three in-depth study sites are representative, but further global analysis is necessary. We demonstrate, using multivariate methods, that the degree of archaeal isoGDGT cyclisation varies in response to temperature and
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Supplementary data will also be hosted on the PANGAEA data repository (www.pangaea.de) under the same title and author details as this publication. We gratefully acknowledge T. Meador and an anonymous reviewer for their valuable comments and time on a previous version of this paper, which greatly improved this manuscript. We also thank Xavier Comas at the Department of Geosciences, Florida Atlantic University, for his hospitality and assistance in accessing and sampling in the Florida
References (133)
- et al.
Bronze Age upland settlement decline in southwest England: testing the climate change hypothesis
Journal of Archaeological Science
(2008) - et al.
Microbial communities in natural and disturbed peatlands: A review
Soil Biology and Biochemistry
(2013) - et al.
Distribution of glycerol ether lipids in halophilic, methanogenic and hyperthermophilic archaea
Organic Geochemistry
(2015) - et al.
An improved method for the analysis of archaeal and bacterial ether core lipids
Organic Geochemistry
(2013) - et al.
Archaeal phospholipids: Structural properties and biosynthesis
Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids
(2017) - et al.
Insoluble prokaryotic membrane lipids in a Sphagnum peat: Implications for organic matter preservation
Organic Geochemistry
(2016) - et al.
Pressure perturbation and differential scanning calorimetric studies of bipolar tetraether liposomes derived from the thermoacidophilic archaeon Sulfolobus acidocaldarius
Biophysical Journal
(2005) - et al.
Impact of climate change on the ecology of the Kyambangunguru crater marsh in southwestern Tanzania during the Late Holocene
Quaternary Science Reviews
(2018) - et al.
Occurrence and distribution of glycerol dialkanol diethers and glycerol dialkyl glycerol tetraethers in a peat core from SW Tanzania
Organic Geochemistry
(2015) - et al.
Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota
Journal of Lipid Research
(2002)
The Lipids of Archaebacteria
Progress in Lipid Research
Lipids of the Archaea: a new tool for bioelectronics
Biosensors and Bioelectronics
Effects of growth phase on the membrane lipid composition of the thaumarchaeon Nitrosopumilus maritimus and their implications for archaeal lipid distributions in the marine environment
Geochimica et Cosmochimica Acta
Influence of temperature, pH, and salinity on membrane lipid composition and TEX86of marine planktonic thaumarchaeal isolates
Geochimica et Cosmochimica Acta
Lipid biosynthesis of Nitrosopumilus maritimus dissected by lipid specific radioisotope probing (lipid-RIP) under contrasting ammonium supply
Geochimica et Cosmochimica Acta
The effect of improved chromatography on GDGT-based palaeoproxies
Organic Geochemistry
Occurrence and distribution of glycerol dialkyl glycerol tetraethers in a French peat bog
Organic Geochemistry
Molecular dynamics simulation study of the effect of glycerol dialkyl glycerol tetraether hydroxylation on membrane thermostability
Biochimica et Biophysica Acta - Biomembranes
Terrestrial environmental change across the onset of the PETM and the associated impact on biomarker proxies: A cautionary tale
Global and Planetary Change
The seasonal and spatial variations of phytoplankton community and their correlation with environmental factors in a large eutrophic Chinese lake (Lake Chaohu)
Ecological Indicators
Structural complexity in isoprenoid glycerol dialkyl glycerol tetraether lipid cores of Sulfolobus and other archaea revealed by liquid chromatography-tandem mass spectrometry
Chemistry and Physics of Lipids
Identification of homoglycerol- and dihomoglycerol-containing isoprenoid tetraether lipid cores in aquatic sediments and a soil
Organic Geochemistry
Differential degradation of intact polar and core glycerol dialkyl glycerol tetraether lipids upon post-depositional oxidation
Organic Geochemistry
Structural diversity and fate of intact polar lipids in marine sediments
Geochimica et Cosmochimica Acta
Predominance of parallel glycerol arrangement in archaeal tetraethers from marine sediments: Structural features revealed from degradation products
Organic Geochemistry
Glycerol configurations of environmental GDGTs investigated using a selective sn2 ether cleavage protocol
Organic Geochemistry
The potential of biomarker proxies to trace climate, vegetation, and biogeochemical processes in peat: A review
Global and Planetary Change
Introducing global peat-specific temperature and pH calibrations based on brGDGT bacterial lipids
Geochimica et Cosmochimica Acta
Archaeal and bacterial H-GDGTs are abundant in peat and their relative abundance is positively correlated with temperature
Geochimica et Cosmochimica Acta
Carbon isotopic compositions of prokaryotic lipids as tracers of carbon cycling in diverse settings
Chemical Geology
The Thaumarchaeota: An emerging view of their phylogeny and ecophysiology
Current Opinion in Microbiology
Identification and distribution of intact polar branched tetraether lipids in peat and soil
Organic Geochemistry
Towards calibration of the TEX86 palaeothermometer for tropical sea surface temperatures in ancient greenhouse worlds
Organic Geochemistry
Pan evaporation and potential evapotranspiration trends in South Florida
Hydrological Processes
Distribution, Activities, and Interactions of Methanogens and Sulfate- Reducing Prokaryotes in the Florida Everglades
Applied and Environmental Microbiology
The Variation of Microbial Communities in a Depth Profile of Peat in the Gahai Lake Wetland Natural Conservation Area
Geomicrobiology Journal
Membrane lipid composition of the moderately thermophilic ammonia-oxidizing archaeon “Candidatus Nitrosotenuis uzonensis” at different growth temperatures
Applied and Environmental Microbiology
Peatlands as scientific archives of past biodiversity
Biodiversity and Conservation
Fossilized glycolipids reveal past oceanic N2 fixation by heterocystous cyanobacteria
Proceedings of the National Academy of Sciences
Unusual butane- and pentanetriol-based tetraether lipids in Methanomassiliicoccus Luminyensis, a representative of the seventh order of methanogens
Applied and Environmental Microbiology
Benthic archaea as potential sources of tetraether membrane lipids in sediments across an oxygen minimum zone
Biogeosciences
A Rapid Method of Total Lipid Extraction and Purification
Canadian Journal of Biochemistry and Physiology
Numerical Ecology with R
Springer
Temperature and pH controls on glycerol dibiphytanyl glycerol tetraether lipid composition in the hyperthermophilic crenarchaeon Acidilobus sulfurireducens
Extremophiles
Canonical correspondence analysis and related multivariate methods in aquatic ecology
Aquatic Sciences
Methanoregula boonei gen. nov., sp. nov., an acidiphilic methanogen isolated from an acidic peat bog
International Journal of Systematic and Evolutionary Microbiology
Methane emissions from wetlands: Biogeochemical, microbial, and modeling perspectives from local to global scales
Global Change Biology
Linking isoprenoidal GDGT membrane lipid distributions with gene abundances of ammonia-oxidizing Thaumarchaeota and uncultured crenarchaeotal groups in the water column of a tropical lake (Lake Challa, East Africa)
Environmental Microbiology
Changing temperature and rainfall gradients in the British Uplands
Climate Research
Vertical profiles of methanogenesis and methanogens in two contrasting acidic peatlands in central New York State, USA
Environmental Microbiology
Cited by (14)
GDGT distribution in tropical soils and its potential as a terrestrial paleothermometer revealed by Bayesian deep-learning models
2023, Geochimica et Cosmochimica ActaLate Holocene climate change in northern Australia inferred from the archaeal lipids in Lake Barrine
2023, Quaternary InternationalGeneral Holocene warming trend in arid Central Asia indicated by soil isoprenoid tetraethers
2022, Global and Planetary ChangeCitation Excerpt :This is further supported by the observation that TEX86-derived MAAT estimate for the topmost soil in the LJW10 section matches well with the measured MAAT rather than GST (see details in Section 4.3). Therefore, instead of the seasonality of soil TEX86, different archaeal ecology and climatic regimes are likely to contribute the diverging TEX86-MAAT relationships in different settings (Naafs et al., 2018; Blewett et al., 2020), which suggests that local calibrations of the TEX86 proxy in soils may be needed. Our results from RDA and hierarchical and variation partitioning for RDA showed that MAP is the second most important environmental variable controlling iGDGT distributions for Mt. Tienshan soils, accounting for a significant amount (44.2%) of the variance in iGDGT distributions independently (Fig. 3a and Table 1).
Glycerol dialkyl glycerol tetraether signatures in tropical mesotidal estuary sediments of Qua Iboe River, Gulf of Guinea
2022, Organic GeochemistryCitation Excerpt :They have been detected in several culture experiments, such as those of methanogenic Euryarchaeota (Knappy et al., 2015; Yoshinaga et al., 2015; Bauersachs et al., 2015), heterotrophic Euryarchaeota (Meador et al., 2014), Crenarchaeota (Knappy et al., 2015) and mesophiles (Bauersachs et al., 2015). They are abundant in tropical peats (Blewett et al., 2020 and references therein), anoxic estuarine sediments (Zhu et al., 2014), deep sea sediment (Zhu et al., 2014), hydrothermal sediments (Reeves et al., 2014) and have relatively high abundances in thermogenic soils (Knappy et al., 2014). The exact factors controlling methylated GDGT productions are not well constrained.