Elsevier

Organic Geochemistry

Volume 148, October 2020, 104080
Organic Geochemistry

Effects of temperature and pH on archaeal membrane lipid distributions in freshwater wetlands

https://doi.org/10.1016/j.orggeochem.2020.104080Get rights and content

Highlights

  • IsoGDGT cyclisation is linked to pH/temperature, but controls are complex.

  • The relative abundance of early/late-eluting isoGDGT isomers changes with pH.

  • Early-eluting isoGDGT isomers can dominate (∼70%) in near-neutral pH wetlands.

  • BDGT producers, possibly methanogens, are likely selected for by near-neutral pH.

  • Me-GDGTs distributions vary, reflecting changing sources/membrane adaptation.

Abstract

Freshwater wetlands harbour diverse archaeal communities and associated membrane lipid assemblages, but the effect of environmental factors (e.g. pH and temperature) on the distribution of these lipids is relatively poorly constrained. Here we explore the effects of temperature and pH on archaeal core-lipid and intact polar lipid (IPL) derived core lipid distributions in a range of wetlands. We focus, not only on the commonly studied isoprenoidal glycerol dialkyl glycerol tetraethers (isoGDGTs), but also widen our analyses to include more recently identified, but relatively widespread, archaeal lipids such as isoGDGT isomers, methylated isoGDGTs (Me-GDGTs), and butanetriol and pentanetriol tetraethers (BDGTs and PDGTs). Based on multivariate analysis and a globally distributed set of wetlands, we find that the degree of isoGDGT cyclisation does increase along with temperature and pH in wetlands. However, and unlike in some other settings, this relationship is obscured in simple scatterplots due to the incorporation of isoGDGTs from highly diverse archaeal sources with multiple ring-temperature or ring-pH relationships. We further show that the relative abundance of early eluting to later eluting isoGDGT isomers increases with pH, representing a previously unknown and seemingly widespread archaeal membrane homeostasis mechanism or taxonomic signal. The distribution and abundance of crenarchaeol, a marker for Thaumarchaeota, demonstrates that in wetlands these Archaea, likely involved in ammonia oxidation, are restricted primarily to the generally drier soil/sediment surface and typically are more abundant in circumneutral pH settings. We identify Me-GDGTs and Me-isoGMGTs (homologs of isoGDGTs and isoGMGTs, but with additional methylation on the biphytanyl chain) as ubiquitous in wetlands, but variation in their abundance and distribution suggests changing source communities and/or membrane adaptation. The high relative abundance of BDGTs and PDGTs in the perennially anoxic part of the peat profile (catotelm), as well as their elevated abundance in a circumneutral pH wetland, is consistent with an important input from their only known culture source, belonging to the methanogenic Methanomassiliicoccales. Our results underline the diversity of archaeal membrane lipids preserved in wetlands and provide a baseline for the use of archaeal lipid distributions in wetlands as tracers of recent or ancient climate and biogeochemistry.

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

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