The role of aluminium in the preservation of microbial biosignatures
|
摘要
Demonstrating the biogenicity of presumptive microfossils in the geological record often requires supporting chemical signatures, including isotopic signatures. Understanding the mechanisms that promote the preservation of microbial biosignatures associated with microfossils is fundamental to unravelling the palaeomicrobiological history of the material. Organomineralization of microorganisms is likely to represent the first stages of microbial fossilisation and has been hypothesised to prevent the autolytic degradation of microbial cell envelope structures. In the present study, two distinct fossilisation textures(permineralised microfossils and iron oxide encrusted cell envelopes)identified throughout iron-rich rock samples were analysed using nanoscale secondary ion mass spectrometry(NanoSIMS). In this system, aluminium is enriched around the permineralised microfossils, while iron is enriched within the intracellularly, within distinct cell envelopes. Remarkably,while cell wall structures are indicated, carbon and nitrogen biosignatures are not preserved with permineralised microfossils. Therefore, the enrichment of aluminium, delineating these microfossils appears to have been critical to their structural preservation in this iron-rich environment. In contrast,NanoSIMS analysis of mineral encrusted cell envelopes reveals that preserved carbon and nitrogen biosignatures are associated with the cell envelope structures of these microfossils. Interestingly, iron is depleted in regions where carbon and nitrogen are preserved. In contrast aluminium appears to be slightly enriched in regions associated with remnant cell envelope structures. The correlation of aluminium with carbon and nitrogen biosignatures suggests the complexation of aluminium with preserved cell envelope structures before or immediately after cell death may have inactivated autolytic activity preventing the rapid breakdown of these organic, macromolecular structures.Combined, these results highlight that aluminium may play an important role in the preservation of microorganisms within the rock record.
Demonstrating the biogenicity of presumptive microfossils in the geological record often requires supporting chemical signatures, including isotopic signatures. Understanding the mechanisms that promote the preservation of microbial biosignatures associated with microfossils is fundamental to unravelling the palaeomicrobiological history of the material. Organomineralization of microorganisms is likely to represent the first stages of microbial fossilisation and has been hypothesised to prevent the autolytic degradation of microbial cell envelope structures. In the present study, two distinct fossilisation textures(permineralised microfossils and iron oxide encrusted cell envelopes)identified throughout iron-rich rock samples were analysed using nanoscale secondary ion mass spectrometry(NanoSIMS). In this system, aluminium is enriched around the permineralised microfossils, while iron is enriched within the intracellularly, within distinct cell envelopes. Remarkably,while cell wall structures are indicated, carbon and nitrogen biosignatures are not preserved with permineralised microfossils. Therefore, the enrichment of aluminium, delineating these microfossils appears to have been critical to their structural preservation in this iron-rich environment. In contrast,NanoSIMS analysis of mineral encrusted cell envelopes reveals that preserved carbon and nitrogen biosignatures are associated with the cell envelope structures of these microfossils. Interestingly, iron is depleted in regions where carbon and nitrogen are preserved. In contrast aluminium appears to be slightly enriched in regions associated with remnant cell envelope structures. The correlation of aluminium with carbon and nitrogen biosignatures suggests the complexation of aluminium with preserved cell envelope structures before or immediately after cell death may have inactivated autolytic activity preventing the rapid breakdown of these organic, macromolecular structures.Combined, these results highlight that aluminium may play an important role in the preservation of microorganisms within the rock record.
Demonstrating the biogenicity of presumptive microfossils in the geological record often requires supporting chemical signatures, including isotopic signatures. Understanding the mechanisms that promote the preservation of microbial biosignatures associated with microfossils is fundamental to unravelling the palaeomicrobiological history of the material. Organomineralization of microorganisms is likely to represent the first stages of microbial fossilisation and has been hypothesised to prevent the autolytic degradation of microbial cell envelope structures. In the present study, two distinct fossilisation textures(permineralised microfossils and iron oxide encrusted cell envelopes)identified throughout iron-rich rock samples were analysed using nanoscale secondary ion mass spectrometry(NanoSIMS). In this system, aluminium is enriched around the permineralised microfossils, while iron is enriched within the intracellularly, within distinct cell envelopes. Remarkably,while cell wall structures are indicated, carbon and nitrogen biosignatures are not preserved with permineralised microfossils. Therefore, the enrichment of aluminium, delineating these microfossils appears to have been critical to their structural preservation in this iron-rich environment. In contrast,NanoSIMS analysis of mineral encrusted cell envelopes reveals that preserved carbon and nitrogen biosignatures are associated with the cell envelope structures of these microfossils. Interestingly, iron is depleted in regions where carbon and nitrogen are preserved. In contrast aluminium appears to be slightly enriched in regions associated with remnant cell envelope structures. The correlation of aluminium with carbon and nitrogen biosignatures suggests the complexation of aluminium with preserved cell envelope structures before or immediately after cell death may have inactivated autolytic activity preventing the rapid breakdown of these organic, macromolecular structures.Combined, these results highlight that aluminium may play an important role in the preservation of microorganisms within the rock record.
引文
Bache, B.W., 1986. Aluminium mobilization in soils and waters. Journal of the Geological Society 143, 699.
Benzerara, K., Menguy, N., Guyot, F., Skouri, F., de Luca, G., Barakat, M., Heulin, T.,2004. Biologically controlled precipitation of calcium phosphate by Ramlibacter tataouinensis. Earth and Planetary Science Letters 228, 439-449.
Beveridge, T.,Meloche, J., Fyfe, W., Murray, R., 1983. Diagenesis of metals chemically complexed to bacteria:laboratory formation of metal phosphates, sulfides, and organic condensates in artificial sediments. Applied and Environmental Microbiology 45.1094-1108.
Brasier, M.D., Antcliffe, J., Saunders, M., Wacey, D., 2015. Changing the picture of Earth's earliest fossils(3.5-1.9 Ga)with new approaches and new discoveries.Proceedings of the National Academy of Sciences 112, 4859-4864.
Cosmidis, J., Benzerara, K., Gheerbrant, E., Esteve, I., Bouya, B., Amaghzaz, M., 2013.Nanometer-scale characterization of exceptionally preserved bacterial fossils in Paleocene phosphorites from Ouled Abdoun(Morocco). Geobiology 11,139-153.
Deleers, M., Servais, J.-P., Wülfert, E., 1985. Micromolar concentrations of Al~(3+)induce phase separation, aggregation and dye release in phosphatidylserinecontaining lipid vesicles. Biochimica et Biophysica Acta(BBA)-Biomembranes 813.195-200.
Deleers, M., Servais, J.-P., Wülfert, E., 1986. Neurotoxic cations induce membrane rigidification and membrane fusion at micromolar concentrations. Biochimica et Biophysica Acta(BBA)-Biomembranes 855, 271-276.
Dorr, J.V.N., 1964. Supergene iron ores of Minas Gerais, Brazil. Economic Geology 59,1203-1240.
Dorr, J.V.N., 1973. Iron-formation in south America. Economic Geology 68,1005-1022.
Exley, C., Birchall, D., 1992. The cellular toxicity of aluminium. Journal of Theoretical Biology 159, 83-98.
Ferris, F.G., Fyfe, W.S., Beveridge, T.J., 1987. Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chemical Geology 63,225-232.
Ferris, F.G., Fyfe, W.S., Beveridge, T.J., 1988. Metallic ion binding by Bacillus subtilis:implications for the fossilization of microorganisms. Geology 16,149-152.
Guida, L, Saidi, Z.. Hughes, M.N., Poole, R.K., 1991. Aluminium toxicity and binding to Escherichia coli Archives of Microbiology 156, 507-512.
Heaney, P.J., Vicenzi, E.P., Giannuzzi, LA., Livi, K.J., 2001. Focused ion beam milling:a method of site-specific sample extraction for microanalysis of Earth and planetary materials. American Mineralogist 86.1094-1099.
Hoppe, P., Cohen, S., Meibom, A., 2013. NanoSIMS:technical aspects and applications in cosmochemistry and biological geochemistry. Geostandards and Geoanalytical Research 37,111-154.
Jacobi, C.M., Carmo, F.F.. 2011. Life-forms, pollination and seed dispersal syndromes in plant communities on ironstone outcrops, SE Brazil. Acta Botanica Brasilica25, 395-412.
Konhauser, K.O., Jones, B., Phoenix, V.R., Ferris, G., Renaut, R.W., 2004. The microbial role in hot spring silicification. AMBIO:A Journal of the Human Environment33, 552-558.
Levett, A., Gagen, E., Shuster, J., Rintoul, L, Tobin, M., Vongsvivut, J., Bambery, K.,Vasconcelos, P., Southam, G., 2016. Evidence of biogeochemical processes in iron duricrust formation. Journal of South American Earth Sciences 71,131-142.
Li, J., Benzerara, K., Bernard, S., Beyssac, 0., 2013. The link between biomineralization and fossilization of bacteria:insights from field and experimental studies.Chemical Geology 359, 49-69.
Li, J., Bernard, S., Benzerara, K., Beyssac, O., Allard, T., Cosmidis, J., Moussou, J., 2014.Impact of biomineralization on the preservation of microorganisms during fossilization:an experimental perspective. Earth and Planetary Science Letters400.113-122.
Londono, S.C., Hartnett, H.E., Williams, LB., 2017. Antibacterial activity of aluminum in clay from the Colombian Amazon. Environmental Science&Technology 51,2401-2408.
Macdonald, T.L., Martin, B.R., 1988. Aluminum ion in biological systems. Trends in Biochemical Sciences 13.15-19.
Marshall, C.P., Emry, J.R., Marshall, A.O., 2011. Haematite pseudomicrofossils present in the 3.5-billion-year-old apex chert. Nature Geoscience 4, 240.
Martin, R.B., 1986. The chemistry of aluminum as related to biology and medicine.Clinical Chemistry 32.1797.
Miot, J., Benzerara, K., Morin, G., Kappler, A., Bernard, S., Obst, M., Férard, C., SkouriPanet, F., Guigner, J.-M., Posth, N., Galvez, M., Brown Jr., G.E., Guyot, F., 2009a.Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochimica et Cosmochimica Acta 73, 696-711.
Miot, J., Benzerara, K., Obst, M., Kappler, A., Hegler, F., Schadler, S., Bouchez, C.,Guyot, F., Morin, G., 2009b. Extracellular iron biomineralization by photoautotrophic iron-oxidizing bacteria. Applied and Environmental Microbiology 75,5586-5591.
Miot, J., Maclellan, K., Benzerara, K., Boisset, N., 2011. Preservation of protein globules and peptidoglycan in the mineralized cell wall of nitrate-reducing, iron(Ⅱ)-oxidizing bacteria:a cryo-electron microscopy study. Geobiology 9,459-470.
Monteiro, H.S., Vasconcelos, P.M., Farley, K.A., Spier, C.A., Mello, C.L, 2014.(U-Th)/He geochronology of goethite and the origin and evolution of cangas. Geochimica et Cosmochimica Acta 131, 267-289.
Oehler, J.H., Schopf, J.W., 1971. Artificial microfossils:experimental studies of permineralization of blue-green algae in silica. Science 174,1229-1231.
Picard, A., Kappler, A., Schmid, G., Quaroni, L, Obst, M., 2015. Experimental diagenesis of organo-mineral structures formed by microaerophilic Fe(II)-oxidizing bacteria. Nature Communications 6.
Preston, L, Shuster, J., Fernández-Remolar, D., Banerjee. N., Osinski, G., Southam, G.,2011. The preservation and degradation of filamentous bacteria and biomolecules within iron oxide deposits at Rio Tinto. Spain. Geobiology 9,233-249.
Riding, R., 2000. Microbial carbonates:the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47,179-214.
Ruan, H.D., Gilkes, R.J., 1996. Kinetics of phosphate sorption and desorption by synthetic aluminous goethite before and after thermal transformation to hematite. Clay Minerals 63.
Salama, W., El Aref, M., Gaupp, R., 2013. Mineral evolution and processes of ferruginous microbialite accretion-an example from the Middle Eocene stromatolitic and ooidal ironstones of the Bahariya Depression, Western Desert, Egypt.Geobiology 11,15-28.
Sch(a|¨)dler, S., Burkhardt, C., Hegler, F., Straub, K., Miot, J., Benzerara, K., Kappler, A.,2009. Formation of cell-iron-mineral aggregates by phototrophic and nitratereducing anaerobic Fe(Ⅱ)-oxidizing bacteria. Geomicrobiology Journal 26,93-103.
Schulze, D.G., Schwertmann, U., 1984. The influence of aluminium on iron oxides; X,Properties of Al-substituted goethites. Clay Minerals 19, 521-539.
Shuster, D.L, Farley, K.A.. Vasconcelos, P.M., Balco, G., Monteiro, H.S., Waltenberg, K.,Stone, J.O., 2012. Cosmogenic 3He in hematite and goethite from Brazilian"canga"duricrust demonstrates the extreme stability of these surfaces. Earth and Planetary Science Letters 329,41-50.
Spier, C., de Oliveira, S., Rosière, C., 2003. Geology and geochemistry of the Aguas claras and pico iron mines, quadrilátero ferrífero, Minas Gerais, Brazil. Mineralium Deposita 38, 751-774.
Westall, F., 1999. The nature of fossil bacteria:a guide to the search for extraterrestrial life.Journal of Geophysical Research:Planets 104,16437-16451.
Zatta, P., Kiss, T., Suwalsky, M., Berthon, G., 2002. Aluminium(Ⅲ)as a promoter of cellular oxidation. Coordination Chemistry Reviews 228, 271-284.
Benzerara, K., Menguy, N., Guyot, F., Skouri, F., de Luca, G., Barakat, M., Heulin, T.,2004. Biologically controlled precipitation of calcium phosphate by Ramlibacter tataouinensis. Earth and Planetary Science Letters 228, 439-449.
Beveridge, T.,Meloche, J., Fyfe, W., Murray, R., 1983. Diagenesis of metals chemically complexed to bacteria:laboratory formation of metal phosphates, sulfides, and organic condensates in artificial sediments. Applied and Environmental Microbiology 45.1094-1108.
Brasier, M.D., Antcliffe, J., Saunders, M., Wacey, D., 2015. Changing the picture of Earth's earliest fossils(3.5-1.9 Ga)with new approaches and new discoveries.Proceedings of the National Academy of Sciences 112, 4859-4864.
Cosmidis, J., Benzerara, K., Gheerbrant, E., Esteve, I., Bouya, B., Amaghzaz, M., 2013.Nanometer-scale characterization of exceptionally preserved bacterial fossils in Paleocene phosphorites from Ouled Abdoun(Morocco). Geobiology 11,139-153.
Deleers, M., Servais, J.-P., Wülfert, E., 1985. Micromolar concentrations of Al~(3+)induce phase separation, aggregation and dye release in phosphatidylserinecontaining lipid vesicles. Biochimica et Biophysica Acta(BBA)-Biomembranes 813.195-200.
Deleers, M., Servais, J.-P., Wülfert, E., 1986. Neurotoxic cations induce membrane rigidification and membrane fusion at micromolar concentrations. Biochimica et Biophysica Acta(BBA)-Biomembranes 855, 271-276.
Dorr, J.V.N., 1964. Supergene iron ores of Minas Gerais, Brazil. Economic Geology 59,1203-1240.
Dorr, J.V.N., 1973. Iron-formation in south America. Economic Geology 68,1005-1022.
Exley, C., Birchall, D., 1992. The cellular toxicity of aluminium. Journal of Theoretical Biology 159, 83-98.
Ferris, F.G., Fyfe, W.S., Beveridge, T.J., 1987. Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chemical Geology 63,225-232.
Ferris, F.G., Fyfe, W.S., Beveridge, T.J., 1988. Metallic ion binding by Bacillus subtilis:implications for the fossilization of microorganisms. Geology 16,149-152.
Guida, L, Saidi, Z.. Hughes, M.N., Poole, R.K., 1991. Aluminium toxicity and binding to Escherichia coli Archives of Microbiology 156, 507-512.
Heaney, P.J., Vicenzi, E.P., Giannuzzi, LA., Livi, K.J., 2001. Focused ion beam milling:a method of site-specific sample extraction for microanalysis of Earth and planetary materials. American Mineralogist 86.1094-1099.
Hoppe, P., Cohen, S., Meibom, A., 2013. NanoSIMS:technical aspects and applications in cosmochemistry and biological geochemistry. Geostandards and Geoanalytical Research 37,111-154.
Jacobi, C.M., Carmo, F.F.. 2011. Life-forms, pollination and seed dispersal syndromes in plant communities on ironstone outcrops, SE Brazil. Acta Botanica Brasilica25, 395-412.
Konhauser, K.O., Jones, B., Phoenix, V.R., Ferris, G., Renaut, R.W., 2004. The microbial role in hot spring silicification. AMBIO:A Journal of the Human Environment33, 552-558.
Levett, A., Gagen, E., Shuster, J., Rintoul, L, Tobin, M., Vongsvivut, J., Bambery, K.,Vasconcelos, P., Southam, G., 2016. Evidence of biogeochemical processes in iron duricrust formation. Journal of South American Earth Sciences 71,131-142.
Li, J., Benzerara, K., Bernard, S., Beyssac, 0., 2013. The link between biomineralization and fossilization of bacteria:insights from field and experimental studies.Chemical Geology 359, 49-69.
Li, J., Bernard, S., Benzerara, K., Beyssac, O., Allard, T., Cosmidis, J., Moussou, J., 2014.Impact of biomineralization on the preservation of microorganisms during fossilization:an experimental perspective. Earth and Planetary Science Letters400.113-122.
Londono, S.C., Hartnett, H.E., Williams, LB., 2017. Antibacterial activity of aluminum in clay from the Colombian Amazon. Environmental Science&Technology 51,2401-2408.
Macdonald, T.L., Martin, B.R., 1988. Aluminum ion in biological systems. Trends in Biochemical Sciences 13.15-19.
Marshall, C.P., Emry, J.R., Marshall, A.O., 2011. Haematite pseudomicrofossils present in the 3.5-billion-year-old apex chert. Nature Geoscience 4, 240.
Martin, R.B., 1986. The chemistry of aluminum as related to biology and medicine.Clinical Chemistry 32.1797.
Miot, J., Benzerara, K., Morin, G., Kappler, A., Bernard, S., Obst, M., Férard, C., SkouriPanet, F., Guigner, J.-M., Posth, N., Galvez, M., Brown Jr., G.E., Guyot, F., 2009a.Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochimica et Cosmochimica Acta 73, 696-711.
Miot, J., Benzerara, K., Obst, M., Kappler, A., Hegler, F., Schadler, S., Bouchez, C.,Guyot, F., Morin, G., 2009b. Extracellular iron biomineralization by photoautotrophic iron-oxidizing bacteria. Applied and Environmental Microbiology 75,5586-5591.
Miot, J., Maclellan, K., Benzerara, K., Boisset, N., 2011. Preservation of protein globules and peptidoglycan in the mineralized cell wall of nitrate-reducing, iron(Ⅱ)-oxidizing bacteria:a cryo-electron microscopy study. Geobiology 9,459-470.
Monteiro, H.S., Vasconcelos, P.M., Farley, K.A., Spier, C.A., Mello, C.L, 2014.(U-Th)/He geochronology of goethite and the origin and evolution of cangas. Geochimica et Cosmochimica Acta 131, 267-289.
Oehler, J.H., Schopf, J.W., 1971. Artificial microfossils:experimental studies of permineralization of blue-green algae in silica. Science 174,1229-1231.
Picard, A., Kappler, A., Schmid, G., Quaroni, L, Obst, M., 2015. Experimental diagenesis of organo-mineral structures formed by microaerophilic Fe(II)-oxidizing bacteria. Nature Communications 6.
Preston, L, Shuster, J., Fernández-Remolar, D., Banerjee. N., Osinski, G., Southam, G.,2011. The preservation and degradation of filamentous bacteria and biomolecules within iron oxide deposits at Rio Tinto. Spain. Geobiology 9,233-249.
Riding, R., 2000. Microbial carbonates:the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47,179-214.
Ruan, H.D., Gilkes, R.J., 1996. Kinetics of phosphate sorption and desorption by synthetic aluminous goethite before and after thermal transformation to hematite. Clay Minerals 63.
Salama, W., El Aref, M., Gaupp, R., 2013. Mineral evolution and processes of ferruginous microbialite accretion-an example from the Middle Eocene stromatolitic and ooidal ironstones of the Bahariya Depression, Western Desert, Egypt.Geobiology 11,15-28.
Sch(a|¨)dler, S., Burkhardt, C., Hegler, F., Straub, K., Miot, J., Benzerara, K., Kappler, A.,2009. Formation of cell-iron-mineral aggregates by phototrophic and nitratereducing anaerobic Fe(Ⅱ)-oxidizing bacteria. Geomicrobiology Journal 26,93-103.
Schulze, D.G., Schwertmann, U., 1984. The influence of aluminium on iron oxides; X,Properties of Al-substituted goethites. Clay Minerals 19, 521-539.
Shuster, D.L, Farley, K.A.. Vasconcelos, P.M., Balco, G., Monteiro, H.S., Waltenberg, K.,Stone, J.O., 2012. Cosmogenic 3He in hematite and goethite from Brazilian"canga"duricrust demonstrates the extreme stability of these surfaces. Earth and Planetary Science Letters 329,41-50.
Spier, C., de Oliveira, S., Rosière, C., 2003. Geology and geochemistry of the Aguas claras and pico iron mines, quadrilátero ferrífero, Minas Gerais, Brazil. Mineralium Deposita 38, 751-774.
Westall, F., 1999. The nature of fossil bacteria:a guide to the search for extraterrestrial life.Journal of Geophysical Research:Planets 104,16437-16451.
Zatta, P., Kiss, T., Suwalsky, M., Berthon, G., 2002. Aluminium(Ⅲ)as a promoter of cellular oxidation. Coordination Chemistry Reviews 228, 271-284.