Trehalose, mannitol and arabitol as indicators of fungal metabolism in Late Cretaceous and Miocene deposits

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Abstract

Trehalose, mannitol and arabitol are the main saccharides of extant fungal metabolism, but their occurrence and distribution in geological materials have rarely been considered. Here, we identify these sugars in Miocene lignites and for the first time in Late Cretaceous mudstones and coals. The co-occurrence of trehalose, mannitol and arabitol in the sedimentary rocks investigated suggests their fungal origin, because these three saccharides are major compounds present in most modern fungi, including the very common mycorrhizal and wood-rotting groups. Therefore, we conclude that these sugars should be treated as new fungal biomarkers (biomolecules) present in geological rocks. Trehalose and mannitol are major compounds in total extracts of the samples and a sum of their concentration reaches 4.6 μg/g of sample. The arabitol concentrations do not exceed 0.5 μg/g, but in contrast to trehalose, the concentration correlates well with mannitol (R2 = 0.94), suggesting that they have the same, translocatory role in fungi. Based on the trehalose vs. mannitol and arabitol distributions in Cretaceous samples and their comparison with data for modern fungi, we preliminarily conclude that the coal seams from the Rakowice Małe (SW Poland) section were formed during warmer climatic periods than the overlying sediments. Furthermore, no DNA could be isolated from the samples of lignites and overlying sediments, whereas it was abundant in the control samples of maple, birch and oak wood degraded by fungi. This indicates an absence of recent fungi responsible for decay in lignites and implies that the saccharide origin is connected with ancient fungi.

Other sugar alcohols and acids like D-pinitol, quinic acid and shikimic acid, were found for the first time in sedimentary rocks, and their source is inferred to be from higher plants, most likely conifers. The preservation of mono- and disaccharides of fungal origins in pre-Palaeogene strata implies that compounds previously thought as unstable can survive for tens to hundreds of millions of years without structural changes in immature rocks unaffected by secondary processes.

Introduction

Biomolecules, natural products of living organisms are relatively rare in sedimentary organic matter (OM). This is mainly connected with the fact that their low stability leads to early metabolic and diagenetic destruction or conversion. Nevertheless, in favorable conditions (low maturation, reducing redox potential, no secondary processes) biomolecules can be preserved hundreds of millions of years, and were occasionally reported from sediments across the Mesozoic and Cenozoic (e.g. Otto and Simoneit, 2001; Otto et al., 2002; Marynowski et al., 2007a, 2007b; Talbot et al., 2016; Rybicki et al., 2017).

Saccharides, ubiquitous biomolecules in both plant and animal kingdoms, are common in marine and terrestrial environments (Klok et al., 1984; Moers et al., 1989; Hernes et al., 1996; Wakeham et al., 1997; Amon and Benner, 2003; Comont et al., 2006; Jia et al., 2008), but were only incidentally described from geological materials older than Holocene (e.g. Moers et al., 1994; Fabbri et al., 2009). However, in euxinic conditions polysaccharides can be preserved through sulfurization processes. Experimental study has shown that the reaction of glucose and cellulose with H2S leads to formation of organic sulfur compounds (Moers et al., 1988). Later, van Kaam-Peters et al. (1998) and Sinninghe Damsté et al. (1998) demonstrated using isotope and molecular studies that sulfurized carbohydrates can constitute an important part of kerogen.

Nonetheless, not all data can be considered as credible. Reports from the sixties about occurrence of sugars in Precambrian and Cambrian rocks should be treated as historical studies showing the detection of contamination by saccharides dissolved and migrated in water (e.g. Palacas et al., 1960; Swain et al., 1970). Only recently Marynowski et al. (2018) identified primary α- and β-glucose in a Middle Jurassic fossil wood and over a dozen mono- and disaccharides in Miocene detritic lignites and xylites. The disaccharides occurrence (sucrose and trehalose) is especially of interest, because this shows that the glycosidic bond between saccharide monomers can survive for millions of years.

The source of saccharides in the geological record is not clear. It is likely, that glucose found in Mesozoic wood and sedimentary rocks could be a remnant of cellulose degradation (Rybicki et al., 2017; Marynowski et al., 2018). Other mono- and disaccharides from Miocene lignites can be degradation products of biopolymers such as hemicellulose and cellulose, but would potentially also occur as free sugars preserved in xylites and detritic coals (Marynowski et al., 2018).

Here we demonstrate the co-occurrence of mannitol, arabitol, trehalose, and other sugars in the Late Cretaceous sections from the Rakowice Małe area (SW Poland), as well as their presence in some Miocene detritic lignites and xylites. We propose that these compounds, when present as dominant saccharides, can be used as indicators of fungal metabolism, as is typical for many modern fungi (e.g. Koide et al., 2000; Simoneit et al., 2004; Hybelbauerová et al., 2008).

Section snippets

Geological settings

The Late Cretaceous sedimentary rocks, exposed in the Rakowice Małe area (sandstone quarry “Rakowiczki”) contain the youngest (Santonian) part of the structural depression of the North-Sudetic Basin. This sedimentary basin comprises rocks of ages from Carboniferous to Cretaceous, and is strictly connected with a suite of structural depressions, which accompanied the European Variscide orogen (Chrząstek and Wojewoda, 2011; Walaszczyk, 2008). The Santonian sedimentary rocks belong to the Czerna

Samples

Two groups of samples were investigated using geochemical methods. The first group was Late Cretaceous (Coniacian/Santonian) samples from the “Rakowiczki” quarry (51°9′56.57”N; 15°32′33.85″E). Series of Santonian sedimentary rocks are exposed above the exploited deposit of Coniacian sandstone, and between them is an erosion hiatus. The thickness of the Santonian sedimentary rocks is 13 m at the sampling location, and they consist mostly of sandstones, dark grey mudstones and shales with coal

Vitrinite reflectance

The dominant maceral in all samples is vitrinite, preserved usually as large, but highly porous fragments. Inertinite was identified in one sample only as compacted / shattered cells. Mean vitrinite reflectance values measured for 5 samples (100 counts each) ranged from 0.39% to 0.45% Rr (Table S1 in Supplementary Material section). Such values are characteristic for lignites to sub-bituminous coals, where the maximum temperature influence on the OM never exceeded 50 °C (Hunt, 1995).

General geochemical data

Total

Primary character of fungi in Late Cretaceous and Neogene samples

The confirmation of the primary origin of fungal saccharides in an investigated geologic section is an important issue, because modern fungi can potentially contaminate sedimentary rocks or even occur in low rank coals (Haider et al., 2015).

That is why we attempted to isolate total DNA from the Cretaceous rock samples and samples of rotten wood of birch, maple and oak as a positive control. The results of the DNA tests clearly show the presence of bacteria and fungi in the samples of rotten

Conclusions

Trehalose, mannitol and arabitol were identified in Late Cretaceous and Miocene sedimentary rocks using GC–MS analysis. Their origin was interpreted as fungal, based on correlation with diverse types of modern fungi. We believe that the co-occurrence of these three saccharides in sediments indicates fungal metabolism and they can be regarded as fungal biomarkers (biomolecules). Other saccharols and sugar acids including: D-pinitol, quinic acid and shikimic acid were found in geological

Acknowledgments

This work was supported by NCN grant 2015/19/B/ST10/00925 to LM. We thank Dr. S. Kurkiewicz for his technical assistance. Adam Tulec (a.k.a. Żółw) is acknowledged for his help during sampling of the Rakowice Małe section.

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