Appraisal of paleoclimate indices based on bacterial 3-hydroxy fatty acids in 20 Chinese alkaline lakes
Introduction
The terrestrial environment is where the majority of climate change impacts will affect human societies. For example, in Asia the strength of the Monsoon impacts regional rainfall and temperature distributions, directly affecting half of humanity (Cook et al., 2010). However, instrumental records are too short to cover likely patterns of climate changes, networks of paleoclimatic reconstructions are required to help understand the climate dynamic. Over recent decades biomarker-based proxies have been developed for reconstructing terrestrial paleo-temperatures from lake archives. Approaches developed initially for the marine environment, including UK'37 and TEX86, have been adapted and tested in lake sediments (Powers et al., 2004, Sun et al., 2018). However, the alkenone compounds utilized for UK'37 are only found in certain lake environments (e.g., Zink et al., 2001, Pearson et al., 2008, Toney et al., 2010). The most extensively studied biomarker approaches for lacustrine environments in the past decade utilize brGDGT compounds (bacterial branched glycerol dialkyl glycerol tetraethers) to reconstruct temperature and pH (e.g., Zink et al., 2010, Pearson et al., 2011, Sun et al., 2011, Loomis et al., 2012, Dang et al., 2018, Russell et al., 2018). However, for brGDGT-based proxies uncertainties remain over: (a) the disparate biological sources and production of brGDGTs in lakes (e.g., Weber et al., 2015, De Jonge et al., 2020) and soils (e.g., De Jonge et al., 2019), (b) the influence of redox conditions (Weber et al., 2018) and (c) seasonality of production (e.g., Loomis et al., 2014, Dang et al., 2018). Several novel terrestrial bacterial biomarker-based proxies have been recently proposed, namely the branched fatty alcohol ratio BNA15 (Huang et al., 2013) as well as those based on heterocyst glycolipids (HG28 and HG30) (Bauersachs et al., 2015, Klages et al., 2020). The BNA15, HG28 and HG30 proxies show promise but have yet to be globally calibrated and widely applied. Thus there is a need for alternative approaches as lake sediments are the most common continental archive for paleoclimate and can yield many complimentary lines of environmental evidence (Castañeda and Schouten, 2011).
The alternative proxies we focus on here are based on the composition of 3-hydroxy fatty acids (3-OH-FAs). 3-OH-FAs are derived from lipopolysaccharides (LPS), the main component of the outer membrane of Gram-negative bacteria, and appear to have significant potential for paleoclimate reconstruction (Wang et al., 2018, Wang et al., 2021). The lipophilic region of LPS, Lipid A, consists mainly of glucosamine units and fatty acids (Wollenweber and Rietschel, 1990), and many of the fatty acids are 3-OH-FAs. Bacterial 3-OH-FAs with carbon numbers from C10 to C18 have a carboxyl group and a hydroxyl group at the β-position. Recently, 3-OH-FAs have been widely studied in different modern environments and geological archives, including soils (Wang et al., 2016, Wang et al., 2021, Yang et al., 2016, Huguet et al., 2019, Véquaud et al., 2021b, Véquaud et al., 2021a), stalagmites (Wang et al., 2012, Wang et al., 2018) and marine environments (Yang et al., 2020). By investigating the latitudinal soil transect on Mt. Shennongjia in central China, Wang et al. (2016) first developed several temperature and pH proxies based on the ratios between branched (iso and anteiso) and normal 3-OH-FAs. These soil-based proxies were successfully applied to a stalagmite in central China to reconstruct independent temperature and hydrological signals for the last 9 kyr (Wang et al., 2018). The proxies were further verified by Huguet et al. (2019) when applied to soil transects from Mt. Rungwe (SW Tanzania) and Mt. Majella (Central Italy). Recently, both linear equations and machine learning tools, such as the Gaussian Process and random forests, have been applied to the development of global calibrations of temperature and pH based on the distribution of 3-OH-FAs in soil samples worldwide (Véquaud et al., 2021b, Wang et al., 2021).
Yang et al. (2020) first investigated 3-OH-FAs profiles in marginal marine settings (in the North Pacific), subject to varying inputs of terrestrial organic matter, and found that 3-OH-FA distributions in marine sediments were distinct from terrestrial soil samples. Specifically, marine samples contained higher relative abundances of anteiso 3-OH-FAs (>20%) compared to soils (<5%) (Yang et al., 2020). Moreover, Yang et al. (2020) found that the previously defined soil temperature proxies, RAN15 (the ratio of anteiso to normal C15 3-OH-FA) and RAN17 (the ratio of anteiso to normal C17 3-OH-FA), were not sensitive to temperature changes in the marine transect they studied. Instead, they proposed RAN13 (the ratio of anteiso to normal C13 3-OH-FA) as a novel sea surface temperature proxy (Yang et al., 2020). These recent investigations suggest that 3-OH-FAs producers in other aquatic environments, including lakes, might be different from those in non-aquatic environments (e.g., soils), challenging the potential for using soil-based 3-OH-FAs as lacustrine climate proxies. Thus the 3-OH-FA distributions, their bacterial precursor populations and potential proxy correlations with temperature and pH need to be fundamentally investigated in lake systems.
Although 3-OH-FAs are present in lake sediments (Wang et al., 2016), the applicability of proxies based on 3-OH-FAs in lacustrine environments has not been systematically investigated. Here we collected samples from 20 Chinese alkaline lakes and surrounding soils from three of the lakes to determine whether soil proxies based on 3-OH-FAs could be applied to lake systems. We compared distributions of 3-OH-FAs from the three lakes and surrounding soils with the gene community compositions in soils from Mt. Yujia, lake sediments from Lake Liangzi to explore the potential sources of 3-OH-FAs to lake sediments. We find unsaturated 3-OH-FA homologs are commonly detected in most of the lake sediments, but with low abundance. Furthermore, we propose novel temperature proxies based on 3-OH-FAs for lake environments and compare them with established brGDGTs temperature proxies from the same sites.
Section snippets
Sampling and environmental parameters
We collected 24 samples of surface sediments from the centers of 20 alkaline freshwater lakes in China (Fig. 1), the same sites investigated by Dang et al., 2016, Dang et al., 2018 for brGDGT distributions. In addition, two soil samples were collected around each of three different lakes (Lake Chagan, Lake Yuqiao and Lake Daihai) to compare the different 3-OH-FAs distributions between the lake sediments and the corresponding catchment soils. The top 0–3 cm of surface sediment was collected with
Environmental parameters
As stated by Dang et al. (2018), lake temperature measurements in the field are transient, and the surface water temperature in most lakes generally reflects air temperature variations (Livingstone et al., 1999, Tierney et al., 2010, Loomis et al., 2011, Magee et al., 2016). Thus, we used MAAT extrapolated from local meteorological stations to explore the temperature influence on 3-OH-FAs. The MAAT varied from 4.9 °C to 17.0 °C across the 24 sites. Lake water pH values fell within a fairly
Biomarker distributions and potential sources of 3-OH-FAs in lake sediments
We continued the approach of Yang et al. (2020), who used a ternary plot to characterize 3-OH-FAs distributions in marine and soil samples, using the sum of anteiso 3-OH-FAs, the sum of iso and normal C10-14 3-OH-FAs, and the sum of iso and normal C15-18 3-OH-FAs as three end-members and included lake sediments as well as published soil and marine sediment data (Wang et al., 2016, Wang et al., 2018, Wang et al., 2021, Huguet et al., 2019, Yang et al., 2020). The ternary diagram (Fig. 3) shows
Conclusions
We investigated 3-OH-FA distributions in Chinese alkaline lakes and found a relatively higher abundance of unsaturated 3-OH-FA homologs in lake sediments compared to soils. We compared the 3-OH-FAs composition (and genetic communities for some sites) among soil, lake, and marine sediments; the results imply a distinct community of 3-OH-FA producers in lake environments with unconstrained contributions from a mixture of in situ production and watershed soil contributions. The Gram-negative
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.
Acknowledgements
We thank the Editors Dr. John Volkman and Dr. George Wolff and two anonymous reviewers for their constructive comments, which greatly improved the quality of this manuscript. This work was supported by the National Natural Science Foundation of China (Grant Nos. 41830319, 41821001, 41807419, 41807317, U20A2094, 91951208, 41773135), the State Key R&D Project of Ministry of Science and Technology (Grant No. 2016YFA0601100), the 111 project (Program of Introducing Talents of Discipline to
References (52)
- et al.
The under-recognized dominance of Verrucomicrobia in soil bacterial communities
Soil Biology and Biochemistry
(2011) - et al.
A review of molecular organic proxies for examining modern and ancient lacustrine environments
Quaternary Science Reviews
(2011) - et al.
Effect of growth hormone on fatty acid oxidation: growth hormone increases the activity of 2,4-dienoyl-CoA reductase in mitochondria
Archives of Biochemistry and Biophysics
(1986) - et al.
Different temperature dependence of the bacterial brGDGT isomers in 35 Chinese lake sediments compared to that in soils
Organic Geochemistry
(2018) - et al.
Lipid biomarker temperature proxy responds to abrupt shift in the bacterial community composition in geothermally heated soils
Organic Geochemistry
(2019) - et al.
Evaluation of 3-hydroxy fatty acids as a pH and temperature proxy in soils from temperate and tropical altitudinal gradients
Organic Geochemistry
(2019) - et al.
Distributions of branched GDGTs in soils and lake sediments from western Uganda: implications for a lacustrine paleothermometer
Organic Geochemistry
(2011) - et al.
Calibration and application of the branched GDGT temperature proxy on East African lake sediments
Earth and Planetary Science Letters
(2012) - et al.
Seasonal variability of branched glycerol dialkyl glycerol tetraethers (brGDGTs) in a temperate lake system
Geochimica et Cosmochimica Acta
(2014) - et al.
Distribution and significance of long-chain alkenones as salinity and temperature indicators in Spanish saline lake sediments
Geochimica et Cosmochimica Acta
(2008)