Recurrence and propagation of past functions through mineral facilitated horizontal gene transfer

Abstract

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.

Reconciling the importance of minerals for propagation of antibiotic resistance genes in the environment

“…In contrast, goethite in higher concentrations caused significant membrane damage, leading to a notable increase in bacterial transformation. [16] Taru et al recently showed that fragmented DNA could be taken up from common mineral surfaces of clays (kaolinite and mica) iron oxides (hematite and goethite) carbonates (calcite) and a non-clay silicate (quartz) [3]. As also observed in the studies of ARg plasmids, the rate of transformation of fragmented DNA varied across the minerals.…”

“…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.…”

“…As also observed in the studies of ARg plasmids, the rate of transformation of fragmented DNA varied across the minerals. Taru et al showed that the DNA-mineral association caused the observed differences in uptake efficiency where a strong DNA-mineral association led to a decrease in uptake frequency [3].…”

“…Recent nano-level investigations have showed that the strength of the DNA mineral association depends on mineral surface topography and the active site density for binding with the molecule in questions [18]. Verma et al showed that the binding affinity between the DNA and the mineral surface and the mobility of the adsorbed molecule scaled with transformation efficiency which highlights that nano-level insight into DNA-mineral binding is an important parameter to consider obtaining mechanistic insight about mineral facilitated transformation [3].…”

A route for long-term DNA preservation through nanoconfinement in smectites

“…2,9 In addition, the absence of exDNA analyses from hot and humid climates is an unfortunate circumstance resulting in, e.g., focus on hominin evolution in northern hemisphere rather than Africa where the evolutionary most novel events took place. 10 Although adsorption to minerals stabilises exDNA against enzymatic digestion, 11 mineral-bound DNA remains available for microbial uptake 12 thus requiring other processes for its long-term preservation. Intercalation, i.e.…”