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| (A) The double stranded structure of DNA. (B) The DNA backbone consists of phosphate and sugar groups. (C) DNA contains 4 different nucleobases bound to the sugar ring: adenine, thymine, cytosine and guanine, that are bound in pairs through hydrogen bonds (H) which give rise to the double helix.
Source publication
A number of studies have highlighted that adsorption to minerals increases DNA longevity in the environment. Such DNA-mineral associations can essentially serve as pools of genes that can be stored across time. Importantly, this DNA is available for incorporation into alien organisms through the process of horizontal gene transfer (HGT). Here we ar...
Contexts in source publication
Context 1
... general, silicates have a low point of zero charge, i.e., they are negatively charged in wide pH range, whereas oxides and hydroxides have high point of zero charge, i.e., they are positively charged in a wide pH range (Figure 2). DNA interacts with minerals through its phosphate backbone (Figures 3A,B), and the nucleobases ( Figure 3C) provide only a limited contribution to adsorption (Vuillemin et al., 2017). The phosphate moieties of DNA are positively charged below ∼pH 2 and can interact directly with negatively charged silicates and basal planes of clay minerals at such low pH values. ...
Context 2
... general, silicates have a low point of zero charge, i.e., they are negatively charged in wide pH range, whereas oxides and hydroxides have high point of zero charge, i.e., they are positively charged in a wide pH range (Figure 2). DNA interacts with minerals through its phosphate backbone (Figures 3A,B), and the nucleobases ( Figure 3C) provide only a limited contribution to adsorption (Vuillemin et al., 2017). The phosphate moieties of DNA are positively charged below ∼pH 2 and can interact directly with negatively charged silicates and basal planes of clay minerals at such low pH values. ...
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Citations
... Specifically, adsorption capacity of minerals for DNA is large in seawater because of high salinity that facilitates attractive interaction, and lower in freshwater because of relatively stronger repulsive forces between DNA and minerals. Therefore, the interplay between surface properties of minerals and environmental conditions under which the adsorption takes place determines how much of the dissolved eDNA can be retained and stored in a particular sediment (Sand & Jelavić, 2018). Implicitly, minerals with a high adsorption capacity for DNA would also be more likely to transport DNA to distant environments. ...
Retrieval of modern and ancient environmental DNA (eDNA) from sediments has revolutionized our ability to study past and present ecosystems. Little emphasis has been placed, however, on the fundamentals of the DNA–sediment associations in environmental settings. Consequently, our understanding of mineralogic controls and geochemical processes that take place on the DNA–sediment interface, and its implications for eDNA taphonomy and provenance, remain extremely limited. Here, we apply interfacial geochemical principles to elucidate how depositional processes and the stability of DNA–sediment associations in different environments can influence our interpretation and identify possible interpretational biases arising from neglecting mineral and geochemical controls on eDNA taphonomy. We use atomic force microscopy to show how interfacial geochemical interactions drive DNA adsorption behavior and we outline how to increase the scope and resolution of ecological interpretations from eDNA by combining mineralogic composition information with experimental adsorption data. We bring the concepts together and propose how to integrate sediment provenance as well as mineralogic and geochemical principles in eDNA taphonomy analysis for improved reconstruction of past ecosystems and monitoring of modern ecosystems from eDNA data. We provide a conceptual understanding of how eDNA taphonomy and sediment provenance can be addressed and further applied to enhance the scope, resolution, and accuracy of modern and past ecological reconstructions based on eDNA data.
... It is well established that mineral surfaces play a role for DNA preservation in the environment, biofilm formation and development, and in DNA transfer from mineral surfaces. Subsequent propagation of mineral adsorbed DNA has received little to no attention despite its implications have been raised [1][2][3]. Here we aim to reconcile that the minerals have a strong influence on biological processes in our ecosystems and showcase implications for the environmental propagation of Arg. ...
The role of mineral surfaces in environmental processes, particularly their influence on DNA preservation, biofilm formation, and genetic transfer, has garnered attention due to its implications for the spread of antibiotic resistance genes (ARg). Despite the recognized significance of mineral-mediated DNA transfer, this mechanism remains poorly understood. Here we investigate the intricate interplay between soil minerals, bacteria, and DNA, to better understand the mechanisms driving ARg propagation in natural environments. We here study the uptake of mineral adsorbed DNA into the natural competent bacteria b. subtilis and further explore the influence of minerals on the viability and subsequent biofilm formation of both b. subtilis and A. baylyi. We further adsorbed DNA to mineral surfaces and allowed biofilm formation while monitoring the propagation of the ARg through out the biofilms. All the results are set in context of mineral surface properties such as surface charge, charge densities and surface area.
Our results showed that the surface properties of the mineral surfaces are highly influencing the transformation efficiencies, viability and biofilm formation where in particular a high number of positive charged surface sites enhance biofilm formation and viability and inhibit transformation. The influence of the mineral surfaces diminishes as the biofilm develops and propagation of mineral adsorbed ARg are seen widely across the mineral surfaces. Our results have implication for mitigations strategies and reconcile mineral surfaces as hot spots for the propagation of antibiotic resistance-which indeed can be driven by transformation in the absence of bacteria carrying the traits. In principle all it takes is one successful transfer event from a mineral adsorbed ARg.
... Adsorption to clay edge sites is very hard to investigate experimentally, and it is currently unclear if clay edge sites would induce fragmentation as seen for calcite. However, several studies have modeled the adsorption of nucleotides to clay edges(Mignon et al., 2019;Pedreira-Segade et al., 2016Sand & Jelavić, 2018) and overall, for the purposes of estimating taphonomy, the edge sites can be expected to behave in a similar manner as the calcite edge sites in terms of binding affinity.The variability in DNA preservation across diverse minerals and chemical contexts underscores the need for careful interpretation in any sedimentary DNA studies. For instance, comparing biodiversity measures from sedimentary profiles with alternating layers of mica and calcite (or minerals with varying degrees of DNA adsorption affinity) necessitates a nuanced understanding of DNA preservation dynamics in each layer. ...
The extraction of environmental DNA (eDNA) from sediments is providing ground‐breaking views of past ecosystems and biodiversity. Despite this rich source of information, it is still unclear which sediments favor preservation and why. Here, we used atomic force microscopy and molecular dynamics simulations to explore the DNA‐mineral interaction to assess how mineralogy and interfacial geochemistry play a role in the preservation of environmental DNA on mineral substrates. We demonstrate that mineral composition, surface topography, and surface charge influence DNA adsorption behavior as well as preservation. Modeling and experimental data show that DNA damage can be induced by mineral binding if there is a strong driving force for adsorption. The study shows that knowledge of the mineralogical composition of a sediment and the environmental conditions can be useful for assessing if a deposit is capable of storing extracellular DNA and to what extent the DNA would be preserved. Our data adds to the understanding of eDNA taphonomy and highlights that, for some mineral systems, fragmented DNA may not represent old DNA.
... Therefore, the interplay between surface properties of minerals and environmental conditions determines how much of the available dissolved eDNA can be retained and stored in a particular sediment type. 9 Inherently minerals with a high adsorption capacity for DNA would also be more likely to transport DNA to distant environments. Thus, the interaction between DNA, minerals, solution and depositional conditions will determine which sediments are more likely to carry DNA and influence which DNAmineral complexes will be preserved in the sedimentary archive. ...
Context for and purpose
Retrieval of modern and ancient environmental DNA (eDNA) from sediments has revolutionized our ability to reconstruct present and past ecosystems. Little emphasis has been placed, however, on the fundamentals of the DNA-sediment associations and, consequently, our understanding of taphonomy and provenance of eDNA in sediments remains extremely limited. If we are to be able to accurately infer community dynamics across time and space from eDNA data, we need to understand how depositional processes and sedimentary associations of DNA molecules in different settings influence our interpretation.
Approach and methods
Here, we introduce interfacial geochemical principles to the field of eDNA and discuss current interpretational biases. We outline a way to increase the scope and resolution of ecological interpretations from eDNA by combining mineralogic composition with experimental adsorption data. We apply distribution coefficients to assess the relationship between the DNA fraction in water columns and DNA fraction sequestered by suspended sediment particles. We further evaluate the challenges with drawing ecological inference using eDNA from sedimentary systems that receive input from different ecosystem types as a consequence of sedimentary processes.
Main results: We show that
The retention of DNA in aqueous environments depends on the mineralogy of sediment particles and on the number of particles loaded in the water column.
DNA attached to sediment particles from distal systems can be deposited in proximal systems and skew the interpretation of the proximal sediment samples.
High particle loading in the water column can deplete suspended DNA and cause inaccurate interpretation of aqueous DNA samples.
High particle loading in surface sediment pore waters enhances sequestration of DNA from benthic communities relative to that of water column communities, resulting in skewed estimates of species richness and abundance from sedimentary DNA.
We discuss how to integrate taphonomy and provenance knowledge into the reconstruction of modern and past ecosystems, and ecosystem monitoring from eDNA data.
Conclusions and the wider implications
Our findings demonstrate that integrating information about eDNA taphonomy and provenance into modern and past ecosystem reconstruction from eDNA data can enhance the scope, resolution and accuracy of our interpretations.
... 30 Here, we explore if mineral preserved DNA can have a broad impact on the evolution of life as suggested by Sand and Jelavic. 31 We tested if fragmented DNA (60 bp) adsorbed to a broad range of environmental relevant minerals can be transferred via uptake to A. baylyi. We inquired if the DNAmineral association, besides being relevant for DNA preservation, also play a role for transformation efficiency, i.e. will a DNA strand loosely associated with a mineral surface be faster to incorporate than a DNA strand tightly adsorbed -if at all? ...
Horizontal gene transfer is the one of the most important drivers of bacterial evolution. Transformation by uptake of extracellular DNA is traditionally not considered to be an effective mode of gene acquisition, simply because extracellular DNA are considered to degrade in a matter of days when it is suspended in e.g. seawater. Mineral surfaces are, however, known to preserve DNA in the environment, and sedimentary ancient DNA studies have solidified there are considerable amounts of fragmented DNA stored in sediments world-wide. Recently the age of stored DNA was increased to at least 2 ma highlighting that sediments represent a rich resource of past traits. It is well established that bacteria can acquire large kilobase DNA molecules adsorbed to mineral surfaces. Here we show that Acinetobacter baylyi can incorporate 60 bp DNA fragments adsorbed to a wide range of common sedimentary minerals. Our recorded transformation frequencies vary with mineral types and scales inversely with mineral surface charge and the ability of the mineral to immobilize the DNA in a liquid environment. We argue that the influence of mineral surface properties introduces interfacial geochemical processes as drivers for evolution and provide sedimentologic processes a central role in the evolutionary avenue of selection.
... The non-living environment in early Earth mainly consists of water, rocks (minerals), and air . Life was supposed to originate in aqueous environment, in which process minerals played key roles (Bernal, 1951;Wächtershäuser, 1992;Pontes-Buarque et al., 2000;Franchi and Gallori, 2005;Gomez et al., 2007;Wächtershäuser, 2007;Xu et al., 2013;Sand and Jelavić, 2018;Ertem, 2021). Growing evidences have demonstrated that the mineral surface is able to concentrate organic molecules, catalyze a variety of reactions, and even serve as reactant (Lahav and Chang, 1976;Ertem and Ferris, 1996;Ferris et al., 1996;Hazen et al., 2001;Ferris, 2002;Zhu et al., 2002;Huang and Ferris, 2003;Miyakawa and Ferris, 2003;Hanczyc et al., 2007;Li et al., 2009;Kawamura et al., 2011;Martra et al., 2014;Liao et al., 2016;Dalai and Sahai, 2019). ...
The first life was believed to emerge in the early Earth via a process involving synthesis of organic compounds and formation of protocells. However, it is still a puzzle how the protocell with hierarchal structure and desirable functions was spontaneously generated in the non-living environment composed of mainly water and minerals. In this work, using muscovite as an example of minerals, we systemically studied the coacervation of poly ( l -lysine) (PLL), quaternized dextran (Q-dextran), and single-stranded oligonucleotide (ss-oligo) on muscovite surface at varying mixing orders. Only when Q-dextran firstly interacts with muscovite surface to form a coating layer, followed by the addition of ss-oligo and PLL, the formed coacervates exhibit distinct and versatile morphologies, including spherical PLL/ss-oligo droplets on the surface, floating PLL/ss-oligo droplets above the Q-dextran/ss-oligo blanket, and PLL/ss-oligo islands surrounded by the Q-dextran/ss-oligo sea. The kinetic pathways to the resulting morphologies are specific in each case. There results suggest that polysaccharide was probably the first biopolymer accumulated on the mineral surface in early Earth. The sugar coating provided a “nest” for protein/peptide and DNA/RNA to from sub-compartments and to further develop advanced functions.
... The integrity of naked DNA depends on many biotic and abiotic factors (Pontiroli et al., 2007) and most naked DNA is degraded within hours to weeks due to the adverse influence of the surrounding environment. However, small amounts of naked DNA may associate with smaller substrate particle sizes, such as minerals in sand and clay, thereby increasing DNA survival and therefore its availability for HGT (see review by Sand and Jelavić, 2018). It is worth noting that DNA fragments of any size can be internalised by competent prokaryotes and may become incorporated into their genome. ...
Gene technology regulators receive applications seeking permission for the environmental release of genetically modified (GM) plants, many of which possess beneficial traits such as improved production, enhanced nutrition and resistance to drought, pests and diseases. The regulators must assess the risks to human and animal health and to the environment from releasing these GM plants. One such consideration, of many, is the likelihood and potential consequence of the introduced or modified DNA being transferred to other organisms, including people. While such gene transfer is most likely to occur to sexually compatible relatives (vertical gene transfer), horizontal gene transfer (HGT), which is the acquisition of genetic material that has not been inherited from a parent, is also a possibility considered during these assessments. Advances in HGT detection, aided by next generation sequencing, have demonstrated that HGT occurrence may have been previously underestimated. In this review, we provide updated evidence on the likelihood, factors and the barriers for the introduced or modified DNA in GM plants to be horizontally transferred into a variety of recipients. We present the legislation and frameworks the Australian Gene Technology Regulator adheres to with respect to the consideration of risks posed by HGT. Such a perspective may generally be applicable to regulators in other jurisdictions as well as to commercial and research organisations who develop GM plants.
... Specialized silica binding protocols, such as SiO 2 + PB buffer and SiO 2 + QG buffer methods, have been widely used to efficiently recover prokaryotic and eukaryotic fragmented and degraded aDNA fragments from sediments and other sample types [6,9,17,33,95]. The SiO 2 + PB buffer method was reported to have better recovery of small DNA fragments than the SiO 2 + QG buffer method [6]; our results are consistent with those findings, despite the results of Sample 4. The site where Sample 4 was collected corresponds to a former paleolake covered by a layer of sandy clay [96], making the recovery of extracellular DNA, and specifically of shorter fragments, particularly challenging due to the strong capacity of clay to absorb and bind DNA molecules [97,98]. In Sample 4, it is possible that the use of Guanidine thiocyanate (QG buffer)-a stronger chaotropic salt compared to guanidine hydrochloride (PB buffer)-could have facilitated a better overall recovery of shorter fragments compared to other protocols. ...
High Throughput DNA Sequencing (HTS) revolutionized the field of paleomicrobiology, leading to an explosive growth of microbial ancient DNA (aDNA) studies, especially from environmental samples. However, aDNA studies that examine environmental microbes routinely fail to authenticate aDNA, examine laboratory and environmental contamination, and control for biases introduced during sample processing. Here, we surveyed the available literature for environmental aDNA projects—from sample collection to data analysis—and assessed previous methodologies and approaches used in the published microbial aDNA studies. We then integrated these concepts into a case study, using shotgun metagenomics to examine methodological, technical, and analytical biases during an environmental aDNA study of soil microbes. Specifically, we compared the impact of five DNA extraction methods and eight bioinformatic pipelines on the recovery of microbial aDNA information in soil cores from extreme environments. Our results show that silica-based methods optimized for aDNA research recovered significantly more damaged and shorter reads (<100 bp) than a commercial kit or a phenol–chloroform method. Additionally, we described a stringent pipeline for data preprocessing, efficiently decreasing the representation of low-complexity and duplicated reads in our datasets and downstream analyses, reducing analytical biases in taxonomic classification.
... The single charge of the phosphate di-ester may also have facilitated attachment to catalytic mineral surfaces, the stereochemical preference for cation binding determining the selection of the mineral surface, thereby generating complex structures destined to be used as biochemical entities [40]. Mineral contact with nucleic acids has also been proposed to play a role in horizontal gene transfer (reviewed in [41]). ...
Phosphate and sulfate groups are integral to energy metabolism and introduce negative charges into biological macromolecules. One purpose of such modifications is to elicit precise binding/activation of protein partners. The physico-chemical properties of the two groups, while superficially similar, differ in one important respect—the valency of the central (phosphorus or sulfur) atom. This dictates the distinct properties of their respective esters, di-esters and hence their charges, interactions with metal ions and their solubility. These, in turn, determine the contrasting roles for which each group has evolved in biological systems. Biosynthetic links exist between the two modifications; the sulfate donor 3′-phosphoadenosine-5′-phosphosulfate being formed from adenosine triphosphate (ATP) and adenosine phosphosulfate, while the latter is generated from sulfate anions and ATP. Furthermore, phosphorylation, by a xylosyl kinase (Fam20B, glycosaminoglycan xylosylkinase) of the xylose residue of the tetrasaccharide linker region that connects nascent glycosaminoglycan (GAG) chains to their parent proteoglycans, substantially accelerates their biosynthesis. Following observations that GAG chains can enter the cell nucleus, it is hypothesized that sulfated GAGs could influence events in the nucleus, which would complete a feedback loop uniting the complementary anionic modifications of phosphorylation and sulfation through complex, inter-connected signalling networks and warrants further exploration.
... One explanation is that the oxidation of Fe during meteorization and diagenesis requires a lower exchange of redox equivalents with respect to the biological mechanisms mediated by Ca and S. 16 The second explanation is that it is possible that in the atmospheric conditions of the Precambrian era, the iron oxides contained in the sediments were formed as rocks, which favored that the first organism is formed in this type of rocks. 17,18 The third explanation is based on the Precambrian lutites formed by pyrite crystals (FeS 2 ); this information indicates that Fe 2+ and sulfide ions were abundant in the seas of that era, which gave rise to the formation of lutites. Interestingly, as a step before the formation of pyrite crystals, the sulfide iron had been produced by the first sulfatereducing bacteria. ...
... Hematite (Fe 3+ ) played a relevant role in the early stage of the oxidizing atmosphere because it precipitated from the upper part of oceans due to its lower solubility compared with Fe 2+ . 17 Although it has been proposed that iron was part of the pioneer organism, it is fundamental to know the structure adopted by that first cell in the presence of iron in the atmospheric conditions prevailing in the Precambrian era. To answer this and other questions, it is indispensable to have a model that will allow extrapolating the first chemical structures of the pioneer organism formed in the Precambrian. ...
The Precambrian era is called the first stage of the Earth history and is considered the longest stage in the geological time scale. Despite its duration, several of its environmental and chemical characteristics are still being studied. It is an era of special relevance not only for its duration but also because it is when a set of conditions gave rise to the first organism. This pioneer organism has been proposed to have been formed by a mineral and an organic part. A chemical element suggested to have been part of the structure of this cell is iron. However, what special characteristic does iron have with respect to other chemical elements to be proposed as part of this first cell? To answer this and other questions, it is indispensable to have a model that will allow extrapolating the first chemical structures of the pioneer organism formed in the Precambrian. In this context, for several decades, in vitro structures chemically formed by silica-carbonates have been synthetized, called biomorphs, because they could emulate living organisms and might resemble primitive organisms. It has been inferred that because biomorphs form structures with characteristic morphologies, they could resemble the microfossils found in the cherts of the Precambrian. Aiming at providing some insight on how iron contributed to the formation of the chemical structures of the primitive organism, we evaluated how iron contributes to the morphology and chemical–crystalline structure during the synthesis of these compounds under different conditions found in the primitive atmosphere. Experimentally, synthesis of biomorphs was performed at four different atmospheric conditions including UV light, nonionizing microwave radiation (NIR-mw), water steam (WS), and CO2 in the presence of Fe²⁺, Fe³⁺, and Fe²⁺/Fe³⁺, obtaining 48 different conditions. The produced biomorphs were observed under scanning electron microscopy (SEM). Afterward, their chemical composition and crystalline structure were analyzed through Raman and IR spectroscopy.
