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

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

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.

Archaea, BDGTs, Biogeochemistry, Crenarchaeol, GDGTs, Isomers, Me-GDGTs, Temperature, Wetlands, pH
0146-6380
Blewett, Jerome
705e9fa1-8d1d-4e94-bdaf-1684e09459a1
Naafs, David
0d093b34-0ed0-45a2-8bbd-269762966af2
Gallego-Sala, A.V.
12e23f4b-4a20-41d6-bf8c-9ef8e19c9165
Pancost, Richard D.
5914e19e-7777-4304-9fd8-86e2e9cfe8a1
Inglis, Gordon
1651196d-916c-43cb-b5a0-9b3ecaf5d664
T-GRES Peat Database Collaborators
Blewett, Jerome
705e9fa1-8d1d-4e94-bdaf-1684e09459a1
Naafs, David
0d093b34-0ed0-45a2-8bbd-269762966af2
Gallego-Sala, A.V.
12e23f4b-4a20-41d6-bf8c-9ef8e19c9165
Pancost, Richard D.
5914e19e-7777-4304-9fd8-86e2e9cfe8a1
Inglis, Gordon
1651196d-916c-43cb-b5a0-9b3ecaf5d664

Blewett, Jerome, Naafs, David, Gallego-Sala, A.V. and Pancost, Richard D. , T-GRES Peat Database Collaborators (2020) Effects of temperature and pH on archaeal membrane lipid distributions in freshwater wetlands. Organic Geochemistry, 148, [104080]. (doi:10.1016/j.orggeochem.2020.104080).

Record type: Article

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.

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Accepted/In Press date: 6 July 2020
e-pub ahead of print date: 10 July 2020
Published date: October 2020
Additional Information: Funding Information: 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 Everglades, and Mari Könönen for samples from Sebangau. J. Blewett thanks G. Inglis for useful discussions. J. Blewett is supported by a NERC GW4+ Doctoral Training Partnership studentship from the Natural Environment Research Council (NE/ L002434/1) and is thankful for the support and additional funding from B.D.A. Naafs acknowledges funding through a Royal Society Tata University Research Fellowship. R. D. Pancost acknowledges the Advanced ERC Project “the greenhouse earth system” (T-GRES; project reference 340923). We also thank the NERC Life Sciences Mass Spectrometry Facility (Bristol) for analytical support and D. Atkinson for help with the sample preparation. Members of the T-GRES Peat Database collaborators are M.J. Amesbury, H. Biester, R. Bindler, J. Blewett, M.A. Burrows, D. del Castillo Torres, F.M. Chambers, A.D. Cohen, S.J. Feakins, M. Gałka, A. Gallego-Sala, L. Gandois, D.M. Gray, P.G. Hatcher, E.N. Honorio Coronado, P.D.M. Hughes, A. Huguet, G.N. Inglis, M. Könönen, F. Laggoun-Défarge, O. Lähteenoja, M. Lamentowicz, R. Marchant, X. Pontevedra- Pombal, C. Ponton, A. Pourmand, A.M. Rizzuti, L. Rochefort, J. Schellekens, F. De Vleeschouwer. CASE partner, Elementar UK Ltd . Publisher Copyright: © 2020
Keywords: Archaea, BDGTs, Biogeochemistry, Crenarchaeol, GDGTs, Isomers, Me-GDGTs, Temperature, Wetlands, pH

Identifiers

Local EPrints ID: 443280
URI: http://eprints.soton.ac.uk/id/eprint/443280
ISSN: 0146-6380
PURE UUID: 04b38c83-12d1-4c99-a30b-29f7667b258b
ORCID for Gordon Inglis: ORCID iD orcid.org/0000-0002-0032-4668

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Date deposited: 20 Aug 2020 16:30
Last modified: 17 Mar 2024 05:49

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Contributors

Author: Jerome Blewett
Author: David Naafs
Author: A.V. Gallego-Sala
Author: Richard D. Pancost
Author: Gordon Inglis ORCID iD
Corporate Author: T-GRES Peat Database Collaborators

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