Influence of environmental parameters on the distribution of bacterial lipids in soils from the French Alps: Implications for paleo-reconstructions
Introduction
Direct measurement of environmental data, such as temperature and precipitation, has been possible for the last two centuries, the so-called “instrumental” period. Beyond this period, it is necessary to use indirect approaches to obtain information on the different environmental parameters. “Indirect” indicators of these parameters – so-called proxies – have thus been developed and used regularly for the last few decades.
Organic biomarkers have been of great interest to the scientific community for the reconstruction of past environments over the last decades (Eglinton and Eglinton, 2008), especially microbial compounds. Microorganisms modify the lipid composition of their membranes (e.g., carbon chain length, number of unsaturations, branching level) in response to variations of environmental parameters (pH, temperature, osmotic pressure; Ernst et al., 2016). Such modifications are considered to maintain a functional fluidity and permeability of the microbial membrane (Singer and Nicolson, 1972, Sinensky, 1974, Hazel and Eugene Williams, 1990, Denich et al., 2003). These microbial lipids can be preserved in soils and sediments and can be used as proxies of past environmental conditions.
In this context, glycerol dialkyl glycerol tetraethers (GDGTs) are a family of microbial lipids widely used for paleoenvironmental reconstructions These compounds are ubiquitous in terrestrial (Weijers et al., 2007, Peterse et al., 2012, De Jonge et al., 2014, Naafs et al., 2017) and aquatic environments (Schouten et al., 2002, Schouten et al., 2012, Powers et al., 2010, Peterse et al., 2015, Weber et al., 2015). They are characterized by aliphatic chains connected to two glycerol units via ether bonds. Two groups of GDGTs – isoprenoid and branched – can be distinguished (Schouten et al., 2013 and references therein). Isoprenoid GDGTs (iGDGTs) are produced by archaea. In contrast, GDGTs with branched chains, but no isoprenoid alkyl chains – so-called branched GDGTs (brGDGTs) – are produced by still unidentified bacteria, although some of them may belong to the phylum Acidobacteria (Sinninghe Damsté et al., 2011, Sinninghe et al., 2014, Sinninghe Damsté et al., 2018). They were discovered in peat (Sinninghe Damsté et al., 2000). The analysis of brGDGTs in a large number of soils distributed worldwide then showed that the relative distribution of these compounds is dependent on environmental parameters; mainly temperature and pH (Weijers et al., 2007, De Jonge et al., 2014, De Jonge et al., 2019).
Despite the wide application of brGDGT indices for paleoenvironmental reconstructions in terrestrial settings (Weijers et al., 2011a, Weijers et al., 2011b, Wang et al., 2017, Coffinet et al., 2018), the derived results must be interpreted with caution, as parameters other than temperature or pH, such as humidity (Huguet et al., 2010, Menges et al., 2014), soil type (Davtian et al., 2016, Mueller-Niggemann et al., 2016), vegetation composition (Weijers et al., 2011a, Weijers et al., 2011b, Naeher et al., 2014, Liang et al., 2019) or seasonality (Huguet et al., 2013) can also have an influences on the relative abundances of brGDGTs. These lipids are the only molecular proxies of temperature and pH available in the terrestrial environment to date, as most of the available proxies have been developed in oceanic environments. Despite improvements in brGDGT analytical methods and use of refined calibration models (De Jonge et al., 2014, Hopmans et al., 2016, Dearing Crampton-Flood et al., 2020), the Root Mean Square Error (RMSE) associated with Mean Annual Air Temperature (MAAT) reconstruction using the global brGDGT calibrations in soils, remains high (>4°C), possibly due to the lack of knowledge on all influencing environmental parameters. The development of new molecular proxies, independent of, and complementary to, brGDGTs, is essential to improve the reliability of environmental reconstructions in terrestrial settings.
Recent studies (Wang et al., 2016, Wang et al., 2018, Huguet et al., 2019, Yang et al., 2020) have unveiled the potential of another family of lipids - 3-hydroxy fatty acids (3-OH FAs) - for temperature and pH reconstructions. 3-OH FAs with 10 to 18 carbon atoms are specifically produced by all Gram-negative bacteria and are bound to the lipopolysaccharide (LPS; main component of the outer membrane) by ester or amide bonds. 3-OH FAs are part of the lipid A, which anchors the LPS in the outer membrane of Gram-negative bacteria. Three types of 3-OH FAs can be distinguished: with normal (i.e., straight and unbranched) or branched carbon chains, either iso or anteiso. These compounds were widely used: (i) to quantify Gram-negative bacteria in clinical studies and detect the presence of endotoxins they release (Wollenweber and Rietschel, 1990, Saraf et al., 1997, Szponar et al., 2002, Szponar et al., 2003, Keinänen et al., 2003) and (ii) to characterize and quantify Gram-negative bacteria communities in environmental samples such as aerosols (Lee et al., 2004, Cheng et al., 2012), dissolved organic matter (Wakeham et al., 2003), or soils (Zelles et al., 1995, Zelles, 1999).
3-OH FAs have been recently proposed as proxies of temperature and pH in terrestrial environments after analysis of these compounds in 26 soils along Mount Shennongjia, China (Wang et al., 2016). New indices were developed, with RAN15 and RAN17 (defined as the ratio of C15 or C17 anteiso 3-OH FAs to normal C15 or C17 3-OH FAs) being correlated with MAAT and RIAN (defined as –log ([normal 3-OH FAs]/[anteiso + iso 3-OH FAs])) being dependent on soil pH.
Significant relationships between 3-OH FA distribution and temperature, as well as pH, were similarly observed along two additional altitudinal transects: Mount Majella in Italy and Mount Rungwe in Tanzania (Huguet et al., 2019). The RAN15/RAN17 indices were negatively correlated to air temperature along the three mountains investigated so far (Wang et al., 2016, Huguet et al., 2019). This suggests that Gram-negative bacteria respond to colder temperatures with an increase in anteiso-C15/C17 vs. n-C15/C17 3-OH FAs in order to maintain a proper fluidity and optimal state of the bacterial membrane, the so-called homeoviscous adaptation mechanism (Sinensky, 1974, Hazel and Eugene Williams, 1990). Nevertheless, the relationships between RAN15 and MAAT along Mts. Shennongjia, Rungwe and Majella showed the same slopes but different intercepts (Wang et al., 2016, Huguet et al., 2019), suggesting that regional calibrations may be more adapted to apply RAN15 as a temperature proxy in soils. In contrast, a significant (R2 = 0.60) combined calibration between RAN17 and MAAT could be established using data from Mts. Shennongjia, Rungwe and Majella (Wang et al., 2016, Huguet et al., 2019). Similarly, RIAN was shown to be strongly negatively correlated with soil pH along the three aforementioned mountains (Wang et al., 2016, Huguet et al., 2019), reflecting a general relative increase in normal homologues compared to branched (iso and anteiso) ones with increasing pH. This mechanism was suggested to reduce the permeability and fluidity of the membrane for the cell to cope with lower pH (Watanabe and Takakuwa, 1984, Lepage et al., 1987, Russell, 1989, Russell et al., 1995, Denich et al., 2003, Beales, 2004). 3-OH FA indices were recently applied to estimate temperature and hydrological changes over the last 10,000 years in a speleothem from China (Wang et al., 2018), showing the potential of 3-OH FAs as independent tools for environmental reconstruction in terrestrial settings. A very recent study based on marine sediments from the North Pacific Ocean suggested that the distribution of 3-OH FAs could also be used to reconstruct sea surface temperature (Yang et al., 2020).
Even though these results are promising, the linear regressions between pH/MAAT data and 3-OH FA indices in terrestrial environments are still based on a rather small dataset (ca. 70 soil samples) and show a large degree of scatter, leading to substantial errors in 3-OH FA-based MAAT and pH reconstitutions (MAAT-RMSE = 5.1 °C; pH-RMSE = 0.56; Huguet et al., 2019). One can anticipate that the distribution of 3-OH FAs in soils is impacted by environmental parameters other than the temperature and pH, as observed for brGDGTs. A full understanding of the environmental parameters (e.g., MAAT, pH, soil moisture, organic carbon and nitrogen content, soil types and vegetation communities) influencing bacterial lipid distribution (3-OH FAs and brGDGTs) in soils is required to increase the reliability of the temperature and pH proxies. Nevertheless, to date, there is no report of a detailed investigation of the environmental controls on 3-OH FA distribution in soils and only a limited number of studies on brGDGTs address this question. The aim of this work is thus to determine and quantify the cumulative effect of environmental parameters on the distribution of both brGDGTs and 3-OH FAs along a composite altitudinal transect in a well-constrained sampling site in the French Alps.
Section snippets
Sites and sampling
Surficial soil samples (0–10 cm depth) were collected in the French Alps in October 2017 along two well-documented (MAAT, soil types and vegetation composition) climate-toposequences: the Bauges massif between 232 and 1,475 m a.s.l (above sea level) and the Lautaret-Galibier massif between 1,540 and 2,700 m a.s.l. (Fig. 1; Supp. Fig. 1). MAAT and a precise description of soil types and vegetation composition are available in this area thanks to an integrated long-term observatory belonging to
Bulk soil properties
The organic carbon content (Corg) shows a wide range of variation - from 1.4% for poorly evolved soils (lithosol) to 49.10% for forest organosol (litter soil) - with an average of 9.7% and a standard deviation of 10.3% (Table 2). Only a minority of soils (n = 4) display high Corg values (>30%). The δ13C values show a unimodal distribution (−26.7‰ ± 2.3‰) and range between −29.9‰ and −24.4‰ (Table 2). The N content of the soil samples is normally distributed (0.7% ± 0.5%; Table 2). Relative soil
Discussion
The distribution of brGDGTs (Weijers et al., 2007, Peterse et al., 2012, De Jonge et al., 2014) and 3-OH FAs (Wang et al., 2016, Huguet et al., 2019) in soils was reported to be influenced mainly by MAAT and soil pH. Therefore, the effect of these two environmental parameters on the relative abundance of 3-OH FAs and brGDGTs in the 49 soils of the French Alps was first investigated.
Conclusions
This study thoroughly investigated the environmental factors controlling the distribution of brGDGTs and 3-OH FAs in soils collected along well-documented altitudinal transects in the French Alps. The influence of local parameters (pH and to a lesser extent soil moisture and grain size, related to vegetation and soil types) on brGDGT and 3-OH FA was more important than MAAT. This likely explains the absence or weak relationships between MAAT and brGDGT/3-OH FA-based indices and stresses the
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
We thank Sorbonne Université for a PhD scholarship to P.V. and the Labex MATISSE (Sorbonne Université) for financial support. The EC2CO program (CNRS/INSU – BIOHEFECT/MICROBIEN) is thanked for funding to the SHAPE project. We thank A. Thibault for assisting in the development of new local calibrations. We are grateful to P. Choler for discussions on alpine vegetation and climate, and for comments on the manuscript. We thank two anonymous reviewers for their constructive comments.
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2023, Chemical GeologyCitation Excerpt :The better performance of RAN15/RAN17 was also found in the warmer Peruvian Andes (6.5–26.4°C, coefficient of determination, R2 = 0.71 for RAN15 and 0.81 for RAN17, both p < 0.05; Véquaud et al., 2021b) and Mt. Rungwe (9.1–25.7°C, R2 = 0.80 for RAN15 and 0.54 for RAN17, both p < 0.05; Huguet et al., 2019) than in the colder Chilean Andes (5.8–9.2°C, R2 = 0.03 for RAN15 and 0.04 for RAN17, both p < 0.05; Véquaud et al., 2021b). However, there was no correlation between RAN15/17 and MAAT in the French Alps (Véquaud et al., 2021a), whereas it is a temperate zone. In addition, only a weak correlation was observed between RAN17 and MAAT in the temperate Mt. Majella (Huguet et al., 2019).
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2022, Organic GeochemistryCitation Excerpt :The dependency between soil chemistry (pH is often the reported parameter) and altitude holds true for several altitudinal transects that have been used to determine the temperature dependency of brGDGT lipids. For instance, Peterse et al. (2009), Coffinet et al. (2014) and Véquaud et al. (2021) report that altitude and pH show a negative correlation (pH range 5.5–7.3, r = –0.48, p = 0.02 (African Mt. Rungwe), pH range 4.4–7.9, r = –0.67, p < 0.01 (Chinese Mt. Gongga), pH range 3.6–7.5, r = –0.44 (French Alps)). Wang et al. (2018) report positive correlations between soil pH and altitude (pH range 3.5–6.0, r2 = 0.68 (Chinese Mt. Fanjing), pH range 5–6.5, r2 = 0.63 (Chinese Mt. Gaoligong)).