DISTRIBUTION OF ANTIBIOTIC RESISTANCE GENES IN THE ENVIRONMENT:
THE ROLE OF MINERAL FACILITATED HORIZONTAL GENE TRANSFER
Combining recent research across disciplines, I see evidence that minerals hold a high and unrecognized potential for enhancing the distribution of the ARg in the environment. Adsorption of ARg to minerals significantly increases the ARg’s lifetime and facilitates their distribution by sedimentary transport processes. In addition, minerals also serve as a) sites for horizontal gene transfer (HGT), b) platforms for microbial growth and, hence 3) act as hot spots for propagation of adsorbed ARg to other microbes. However, some minerals and ARg are bound more strongly than others and various bacteria have different affinities toward various minerals. Those variations in affinity are poorly quantified but vital for predicting the distribution of ARg in the environment.
Bacterial colony formation.
Image by Lisselotte Jauffred (collaborator from NBI)
The spread of antibiotic resistance genes (ARg) is a worldwide health risk1 and is no longer only a clinical issue. Vast reservoirs of ARg are found in natural environments2–4 such as soils, sediments and oceans. The emergence and release of ARg to the environment is in particular caused by extended use of antibiotics in farming, e.g. where the genes dissipate from the manure.5 Once in the environment, the ARg are surprisingly rapidly propagated. It is well known that the ARg are distributed to neighbour bacteria through processes of both cell sharing or through horizontal gene transfer (HGT) where one species acquirer resistance from another.6,7 Most HGT responsible for the spread of ARg are assumed to be through direct microbe-microbe contact. However, I find that the outcome of non-contact transfer is grossly underestimated. In the HGT mechanism called “Transformation”, free ARg in suspension or adsorbed to a mineral can be picked up and incorporated into non-related organisms. Considering that free DNA only can survive for a few weeks in sea- and freshwater environments,8–10 any HGT from free DNA can rightly be assumed to be local, but if the DNA gets adsorbed to a mineral, it can survive for several hundred thousands of years.11–14 If this also holds for ARg, then minerals offer a potent mechanism for distributing ARg through our environments my means of sedimentary processes.
Publications
Published peer reviewed book chapters
J. D. Rodriguez-Blanco, K. K. Sand, L. G. Benning, 2017. ACC and Vaterite as Intermediates in the Solution-Based Crystallization of CaCO3. In: New Perspectives on Mineral Nucleation and Growth, A. E. S. V. Driessche, M. Kellermeier, L. G. Benning, D. Gebauer, Eds. (Springer International Publishing, 2017), pp. 93–111.
Published peer reviewed book papers
Kjær K.H., Pedersen M.W., De Sanctis B, De Cahsan B, Korneliussen TS, Michelsen CS, Sand K.K., Jelavić S …Willerslev, E. 2022. A 2-million-year-old ecosystem in Greenland uncovered by environmental DNA. Nature, (7939), 283–91.
Jelavić S, Thygesen LG, Magnin V, Findling N, Müller S, Meklesh V, and Sand K.K. 2022. Soot and charcoal as reservoirs of extracellular DNA. Peer Community J, Ecotox Env Chem
Boschker, H.T.S, Cook, P.L. M. […] Meysman F. J. R. 2021. Efficient long-range conduction in cable bacteria through nickel protein wires. Nature Communications, (12), 3396
Jelavić, S., Mitchell, A. and Sand, K.K. 2020. Fate of organic compounds during transformation of ferrihydrite in iron formations. Geochemical perspective letters.
Sand, K.K., Jelavić, S., Dobberschütz, S., Ashby, P., Marshall, M., Didericksen, K., Stipp, S.L.S., Friddle, R., DeYoreo, J.J. 2020. Mechanistic insight into biopolymer induced iron oxide mineralization through quantification of molecular bonding. Nanoscale Advances, (2), 3323-3333.
Nielsen, A., Mitchell, A. C., Stipp, S. L. S.; Zuckermann. R. and Sand, K. K. 2020. Thermodynamic and Kinetic Parameters for Calcite Nucleation on Peptoid and Model Scaffolds: A Step toward Nacre Mimicry. Crystal growth and design, (20), 3762–3771.
Weihe, S. Mangayayam, M, Sand, K.K, Tobler, D. 2019. Hematite crystallization in the presence of organic matter: impact on crystal properties and bacterial dissolution. ACS Earth and Space Chemistry. (3), 510-518.
Sand, K.K. and Jelavić, S. 2018. Mineral facilitated horizontal gene transfer: A new principle for evolution of life? Frontiers in Geomicrobiology (9).
Dobberschütz, S., Nielsen, M., Sand, K.K., Civioc, R., Bovet, N., Stipp S.L.S. 2018. The mechanisms of crystal growth inhibition by organic and inorganic inhibitors. Nature Communications, (9), 2041-1723.
Jelavić, S., Hassenkam, T., Tobler, D.J., Stipp, S.L.S., Sand, K.K. 2017. Prebiotic RNA polymerisation: nucleotide adsorption and polymerisation on clay mineral surfaces. Chemical Communications, (53), 12700-12703.
Sand, K. K., Pedersen, C. S., Dobberschütz, S., Matthiesen, J., Stipp, S. L. S. 2017. Controlling Biomineralisation with Cations. Nanoscale, (9), 12925-12933.
Sand, K. K., Friddle, R. W., DeYoreo, J. J. 2017. Quantifying the Free Energy Landscape between Polymers and Minerals. Scientific Reports, Nature research. (7), 2045-2322.
Nielsen, M. R., Sand, K.K., Rodriguez-Blanco, J. D., Bovet, N., Dalby, K. N., J., G. Stipp, S. L. S. 2016. Inhibition of Calcite Growth: Combined effects of Mg2+ and SO42-. Crystal Growth and Design, (11), 6199-6207.
Andersson, M.P., Dobberschütz, S., Sand, K.K., Tobler, D., DeYoreo, J.J., Stipp, S.L.S. 2016. A microkinetic model of calcite growth. Angewandte. (37), 11086-90.
Sand, K.K., Tobler, D., Dobberschütz, S., Larsen, K., Makovicky, E., Andersson, M., Wolthers, M., Stipp, S.L.S. 2016. Calcite Growth Kinetics: Dependence on Saturation Index, Ca2+:CO3- Activity Ratio, and Surface Atomic Structure. Crystal Growth and Design. (7), 3602–3612.
Tobler, D.J., Rodriguez-Blanco, J.D, Dideriksen, K., Bovet, N. Sand, K.K. and Stipp, S.L.S. 2015. Citrate Effects on Amorphous Calcium Carbonate (ACC) Structure, Stability and Crystallization. Advanced Functional Materials. (20), 3081-3090.
Andersson, M.P., Hem, C., Schultz, L., Nielsen, J., Pedersen, C.S., Sand, K.K., Okhrimenko, D. Johnson, A. and S.L.S. Stipp. 2014. Infrared Spectroscopy and Density Functional Theory Investigation of Calcite, Chalk, and Coccoliths—Do We Observe the Mineral Surface? The Journal of Physical Chemistry A, (118), 10720-10729.
Sand, K.K., Pedersen, C. S., Sjöberg, S., Nielsen, J. W., Makovicky, E. & Stipp, S. L. S. 2014. Biomineralization: The long term effectiveness of polysaccharides on the growth and dissolution of calcite. Crystal Growth & Design, (14), 5486-5494.
Tobler, D. J., Blanco, J. D. R., Dideriksen, K., Sand, K.K., Bovet, N., Benning, L. G. and Stipp, S. L. S. 2014. The Effect of Aspartic Acid and Glycine on Amorphous Calcium Carbonate (ACC) Structure, Stability and Crystallization. Procedia Earth and Planetary Science, (10), 143-148.
Nielsen, J.W., Sand, K.K., Pedersen, C.S., Willemoes, M. and Stipp, S.L.S. 2012. Polysaccharide effect on calcite growth: The influence of composition and branching. Crystal Growth and Design, (10), 4906–4910.
Sand, K.K., Rodriguez-Blanco, J.D., Makovicky, E., Benning, L.G. and Stipp S. L. S. 2012. Aragonite growth in water-alcohol mixtures: Classical or nonclassical crystallization? MRS Fall conference proceedings, mesf11-1419-nn01-08.
Sand, K.K., Rodriguez-Blanco, J. D., Makovicky, E., Benning, L.G. and Stipp S.L.S. 2012. Crystallization of CaCO3 in water-alcohol mixtures: Spherulitic growth, polymorph stabilization and morphology change. Crystal Growth and Design, (12) 845-853.
Cooke, D., Gray, R., Sand, K.K., Stipp, S.L.S. and Elliott, J. 2010. The interaction of ethanol and water with the {10.4} surface of calcite. Langmuir, (26), 14520-14529.
Sand, K.K., Yang, M., Makovicky, E., Cooke, D., Hassenkam, T., Bechgaard, K., Stipp, S.L.S. 2010. Binding of ethanol on calcite: The role of the OH bond and its relevance to biomineralization. Langmuir, (26), 15239-15247.
Sand, K.K., Waight, T.E., Pearson, D.G., Nielsen, T.F.N., Makovicky, E. and Huchison, M.T. 2009. The lithospheric mantle below southern West Greenland: a geothermobarometric approach to diamond potential and mantle stratigraphy. Lithos, (112), 1155-1166.
Nielsen, T.F.D., Jensen, S.M., Secher, K. and Sand, K.K. 2009. Distribution of kimberlite and ailikite in the Diamond Province of southern West Greenland: regional perspective based on groundmass mineral chemistry and bulk compositions. Lithos, (112), 358-371.
Steenfelt, A., Jensen, S.M., Nielsen, T.F., and Sand, K.K. 2009. Provinces of ultramafic lamprophyre dykes, kimberlite dykes and carbonatite in West Greenland characterised by minerals and chemical components in surface media. Lithos, (112), 116-123.
Steenfelt, A., Jensen, S.M., Nielsen, T.F.D., Sand, K.K. and Secher, K. 2009. Diamonds and lithospheric mantle properties in the Neoproterozoic igneous province of southern West Greenland. Geological Survey of Denmark and Greenland Bulletin 17, Review of Survey activities 2008: 65-69.
Nielsen, T.F.D. & Sand, KK. 2008. The Majuagaa kimberlite dike, Maniitsoq region, West Greenland: constraint for an Mg-rich silicocarbonatite melt composition from groundmass mineralogy and bulk composition. Canadian Mineralogist, (46), 1043-1061.
Published non-peer reviewed book chapters
Sand, K.K., Nielsen, T.F.D., Secher, K. and Steenfelt, A. 2007. Kimberlite and carbonatite exploration in southern West Greenland; Summary of previous activities and recent work by the kimberlite research group at the Geological Survey of Denmark and Greenland. In: Vladykin, N. (Editor), Alkaline magmatism, its sources and plumes. Publishing House of the Institute of Geography, Irkutsk, Napoli, 127-140.
Preprints
Freeman, C. L., Dieudonne, L., Agbaje, O. B. A., Zure, M., Sanz, J. Q., Collins, M. J., Sand, K. K. Survival of Environmental DNA in Sediments: Mineralogic Control on DNA Taphonomy. bioRxiv January 21, 2023, p 2020.01.28.922997.
Sand, K. K., Jelavic, S., Kjaer, K. H., Prohaska, A. Importance of eDNA Taphonomy and Provenance for Robust Ecological Inference: Insights from Interfacial Geochemistry. bioRxiv January 25, 2023, p 2023.01.24.525431. To be submitted to Environmental DNA March 2023.
Verma, T., Hendiani, S., Andersen, S. B., Burmoelle, M., Sand, K. K. Sedimentary DNA Can Influence Evolution: Establishing Mineral Facilitated Horizontal Gene Transfer as a Route to Bacterial Fitness. bioRxiv January 24, 2023, p 2023.01.24.525235. https://doi.org/10.1101/2023.01.24.525235.To be submitted to Nature Geoscience March 2023.
Hendiani, S., Hansen, M.F., Kontopoulos, I.,Verma. T., Pucetaite, M., Burmølle, M., Ramstaedt, M. and Sand. K.K. Fundamentals of biofilm formation in soil: From functionalized self-assembled monolayers to rewilding. bioRxiv January 31, 2023, p 2023.01.30.526320. https://doi.org/10.1101/2023.01.30.526320.
Non-Peer reviewed contributions
Sand, K.K 2022. The role of mineral surfaces for DNA translocation in the environment. Cancer, multicellular and complex systems, Lund 5th – 7th of Sept.
Freeman, C. L., Dieudonne, L., Collins, M. J. and Sand, K. K. 2021. Survival of Environmental DNA in Natural. Environments: Surface Charge and Topography of Minerals as Driver for DNA Storage. Goldschmidt Abstract, Lyon 4th-9th of July
Jelavić, S., Mitchell, A, Sand, K.K. 2021. Implications of ferrihydrite transformation for the fate of organic compounds in Precambrian iron formations. Goldschmidt Abstract, Lyon 4th-9th of July
Kontopoulos, I., Sanz, J.Q., Sand, K.K. 2021. Adsorption characteristics of ssDNA and dsDNA onto mineral surfaces: implications for DNA preservation in sedimentary archives. Goldschmidt Abstract, Lyon 4th-9th of July
Kontopoulos, I., Sanz, J.Q., Sand, K.K. 2021. The effect of surface charge and background electrolytes on the adsorption characteristics of DNA to mineral surfaces. Abstract for 9th international symposium on biomolecular archaeology, Toulouse, 1st-4th of June.
Kontopoulos, I., Sanz, J.Q., Sand, K.K. 2021. Visualisation of DNA adsorption to mineral surfaces using atomic force microscopy. Abstract for Ancient Biomolecules of Plants, Animals, and Microbes. Virtual Conference, 29th-31st of March.
Jelavić, S., Dieudonné, L., Sanz, J.Q., Sand, K.K. 2020. Do minerals play a role in the evolution of life? - Quantification of DNA-mineral interactions. 2020. Abstract for The European Microscopy Congress, Copenhagen 23rd – 28th of August.
Jelavić, S., Sanz, J.Q., Persson, P., Sand K.K. 2020. Kinetics of DNA adsorption and desorption from minerals. Goldschmidt Abstract, Hawaii 21th-26th of June.