Ultrahigh-resolution imaging of biogenic phosphorus and molybdenum in palaeoproterozoic gunflint microfossils.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
20 Sep 2024
20 Sep 2024
Historique:
received:
12
06
2024
accepted:
04
09
2024
medline:
21
9
2024
pubmed:
21
9
2024
entrez:
20
9
2024
Statut:
epublish
Résumé
Phosphorus and molybdenum play important roles in the formation of microbial cell structures and specific enzymes crucial for metabolic processes. Nevertheless, questions remain about the preservation of these elements within ancient microfossils. Here, we present shape-accurate ion images capturing phosphorus and molybdenum on Palaeoproterozoic filamentous microfossils by pioneering a methodology using lateral high-resolution secondary ion mass spectrometry. Introducing electrically conductive glass for mounting isolated microfossils facilitated clearer observations with increased secondary ion yields. Phosphorus was detected along the contours of microfossils, providing direct evidence of phospholipid utilization in the cell membrane. Trace amounts of molybdenum were detected within microfossil bodies, suggesting potential remnants of molybdenum-bearing proteins, such as nitrogenase. These findings align with the hypothesized cyanobacterial origin of filamentous gunflint microfossils. Our methodology introduces a groundbreaking tool for obtaining crucial insights into the cellular evolution and metabolic pathways of microorganisms, allowing comparisons of their morphological characteristics.
Identifiants
pubmed: 39304716
doi: 10.1038/s41598-024-72191-8
pii: 10.1038/s41598-024-72191-8
doi:
Substances chimiques
Molybdenum
81AH48963U
Phosphorus
27YLU75U4W
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
21780Subventions
Organisme : Japan Society for the Promotion of Science
ID : 22K03790
Organisme : Japan Society for the Promotion of Science
ID : 22H00163
Organisme : Japan Society for the Promotion of Science,Japan
ID : 23K19065
Informations de copyright
© 2024. The Author(s).
Références
Tyler, S. A. & Barghoorn, E. S. Occurrence of structurally preserved plants in pre-Cambrian rocks of the Canadian shield. Science 119, 606–608 (1954).
pubmed: 17777442
doi: 10.1126/science.119.3096.606
Barghoorn, E. S. & Tyler, S. Microorganisms from the gunflint chert. Science 147, 3658 (1965).
doi: 10.1126/science.147.3658.563
Javaux, E. J. & Lepot, K. The paleoproterozoic fossil record: implications for the evolution of the biosphere during Earth’s middle-age. Earth Sci. Rev. 176, 68–86 (2018).
doi: 10.1016/j.earscirev.2017.10.001
Lepot, K. Signatures of early microbial life from the archean (4 to 25° Ga) eon. Earth Sci. Rev. 209, 103296 (2020).
doi: 10.1016/j.earscirev.2020.103296
Awramik, S. M. & Barghoorn, E. S. The gunflint microbiota. Precam. Res. 5, 121–142 (1977).
doi: 10.1016/0301-9268(77)90025-0
Planavsky, N. et al. Iron-oxidizing microbial ecosystems thrived in late paleoproterozoic redox-stratified oceans. Earth Planet. Sci. Lett. 286, 230–242 (2009).
doi: 10.1016/j.epsl.2009.06.033
Sasaki, K., Ishida, A., Takahata, N., Sano, Y. & Kakegawa, T. Evolutionary diversification of paleoproterozoic prokaryotes: New microfossil records in 1.88 Ga gunflint formation. Precam. Res. 380, 106798 (2022).
doi: 10.1016/j.precamres.2022.106798
House, C. H. et al. Carbon isotopic composition of individual Precambrian microfossils. Geology 28(8), 707–710 (2000).
pubmed: 11543502
doi: 10.1130/0091-7613(2000)28<707:CICOIP>2.0.CO;2
Wacey, D. et al. Nanoscale analysis of pyritized microfossils reveals differential heterotrophic consumption in the ̃1 9 Ga gunflint chert. Proc. Nat. Acad. Sci. USA 110(20), 8020–8024 (2013).
pubmed: 23630257
pmcid: 3657779
doi: 10.1073/pnas.1221965110
Williford, K. H. et al. Preservation and detection of microstructural and taxonomic correlations in the carbon isotopic compositions of individual precambrian microfossils. Geochim. Cosmochim. Acta 104, 165–182 (2013).
doi: 10.1016/j.gca.2012.11.005
Wacey, D., Saunders, M., Kong, C., Brasier, A. & Brasier, M. 3.46 Ga apex chert ‘microfossils’ reinterpreted as mineral artefacts produced during phyllosilicate exfoliation. Gondwana Res. 36, 296–313 (2016).
doi: 10.1016/j.gr.2015.07.010
Lepot, K. et al. Iron minerals within specific microfossil morphospecies of the 1.88 Ga Gunflint Formation. Nat. Commun. 8, 14890 (2017).
pubmed: 28332570
pmcid: 5376642
doi: 10.1038/ncomms14890
De Gregorio, B. T., Sharp, T. G., Flynn, G. J., Wirick, S. & Hervig, R. L. Biogenic origin for earth’s oldest putative microfossils. Geology 37(7), 631–634 (2009).
doi: 10.1130/G25683A.1
Lukmanov, R. A. et al. Multiwavelength ablation/ionization and mass spectrometric analysis of 1.88 Ga gunflint chert. Astrobiology 22(4), 369–386 (2022).
pubmed: 35196459
doi: 10.1089/ast.2019.2201
Tribovillard, N., Algeo, T. J., Lyons, T. & Riboulleau, A. Trace metals as paleoredox and paleoproductivity proxies: An update. Chem. Geol. 232(1–2), 12–32 (2006).
doi: 10.1016/j.chemgeo.2006.02.012
Zerkle, A. L., House, C. H., Cox, R. P. & Canfield, D. E. Metal limitation of cyanobacterial N2 fixation and implications for the precambrian nitrogen cycle. Geobiology 4(4), 285–297 (2006).
doi: 10.1111/j.1472-4669.2006.00082.x
Anbar, A. D. et al. A whiff of oxygen before the great oxidation event?. Science 317, 1903–1906 (2007).
pubmed: 17901330
doi: 10.1126/science.1140325
Parnell, J., Spinks, S., Andrews, S., Thayalan, W. & Bowden, S. High molybdenum availability for evolution in a mesoproterozoic lacustrine environment. Nat. Commun. 6, 6996 (2015).
pubmed: 25988499
doi: 10.1038/ncomms7996
Guo, Z., Peng, X., Czaja, A. D., Chen, S. & Ta, K. Cellular taphonomy of well-preserved Gaoyuzhuang microfossils: A window into the preservation of ancient cyanobacteria. Precam. Res. 304, 88–98 (2018).
doi: 10.1016/j.precamres.2017.11.007
Delarue, F. et al. Out of rock: A new look at the morphological and geochemical preservation of microfossils from the 3.46 Gyr-old strelley pool formation. Precam. Res. 336, 105472 (2020).
doi: 10.1016/j.precamres.2019.105472
Pett-Ridge, J. & Weber, P. K. NanoSIP: NanoSIMS applications for microbial biology. Microb. Syst. Biol. Methods Protoc. https://doi.org/10.1007/978-1-61779-827-6_13 (2012).
doi: 10.1007/978-1-61779-827-6_13
Grey, K. & Sugitani, K. Palynology of archean microfossils (ca. 3.0 Ga) from the Mount grant area, pilbara craton, Western Australia: Further evidence of biogenicity. Precam. Res. 173, 60–69 (2009).
doi: 10.1016/j.precamres.2009.02.003
Slaveykova, V. I., Guignard, C., Eybe, T., Migeon, H. N. & Hoffmann, L. Dynamic NanoSIMS ion imaging of unicellular freshwater algae exposed to copper. Anal. Bioanal. Chem. 393, 583–589 (2009).
pubmed: 18985325
doi: 10.1007/s00216-008-2486-x
Sanz-Luque, E., Bhaya, D. & Grossman, A. R. Polyphosphate: A multifunctional metabolite in cyanobacteria and algae. Front. Plant Sci. 11, 93 (2020).
doi: 10.3389/fpls.2020.00938
Jackson, M. D. & Denu, J. M. Molecular reactions of protein phosphatases—Insights from structure and chemistry. Chem. Rev. 101, 2313–2340 (2001).
pubmed: 11749375
doi: 10.1021/cr000247e
Edwards, C. T., Pufahl, P. K., Hiatt, E. E. & Kyser, T. K. Paleoenvironmental and taphonomic controls on the occurrence of paleoproterozoic microbial communities in the 1.88 Ga ferriman group labrador trough Canada. Precam. Res 212, 91–106 (2012).
doi: 10.1016/j.precamres.2012.04.020
Muscente, A. D., Hawkins, A. D. & Xiao, S. Fossil preservation through phosphatization and silicification in the ediacaran doushantuo formation (South China): A comparative synthesis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 434, 46–62 (2015).
doi: 10.1016/j.palaeo.2014.10.013
Hanczyc, M. M., Fujikawa, S. M. & Szostak, J. W. Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302(5645), 618–622 (2003).
pubmed: 14576428
pmcid: 4484575
doi: 10.1126/science.1089904
Alleon, J. et al. Molecular preservation of 1.88 Ga gunflint organic microfossils as a function of temperature and mineralogy. Nat. Commun. https://doi.org/10.1038/ncomms11977 (2016).
doi: 10.1038/ncomms11977
pubmed: 27312070
pmcid: 4915024
Igisu, M. et al. Changes of aliphatic C–H bonds in cyanobacteria during experimental thermal maturation in presence or absence of silica as evaluated by FTIR microspectroscopy. Geobiology 16, 412–428 (2018).
pubmed: 29869829
doi: 10.1111/gbi.12294
Demoulin, C. F. et al. Polysphaeroids filiformis, a proterozoic cyanobacterial microfossil and implications for cyanobacteria evolution. iScience 27, 108865 (2024).
pubmed: 38313056
pmcid: 10837632
doi: 10.1016/j.isci.2024.108865
Jonkers, H. M., van der Maarel, M. J. E. C., Gemerden, H. V. & Hansen, T. A. Dimethylsulfoxide reduction by marine sulfate-reducing bacteria. FEMS Microbiol. Lett. 136, 283–287 (1996).
doi: 10.1111/j.1574-6968.1996.tb08062.x
Tucker, M. D., Barton, L. L. & Thomson, B. M. Reduction and immobilization of molybdenum by desulfovibrio desulfuricans. J. Environ. Qual. 26, 1146–1152 (1997).
doi: 10.2134/jeq1997.00472425002600040029x
Tucker, M. D., Barton, L. L. & Thomson, B. M. Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilized in polyacrylamide gels. J. Ind. Microbiol. Biotechnol. 20, 13–19 (1998).
pubmed: 9565467
doi: 10.1038/sj.jim.2900472
Hensel, M., Hinsley, A. P., Nikolaus, T., Sawers, G. & Berks, B. C. The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol. Microbiol. 32, 275–287 (1999).
pubmed: 10231485
doi: 10.1046/j.1365-2958.1999.01345.x
Kappler, U. et al. Sulfite: Cytochrome c oxidoreductase from Thiobacillus novellus. Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J. Biol. Chem. 275, 13202–13212 (2000).
pubmed: 10788424
doi: 10.1074/jbc.275.18.13202
Burns, J. L. & DiChristina, T. J. Anaerobic respiration of elemental sulfur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phsA gene of Salmonella enterica serovar typhimurium LT2. Appl. Environ. Microbiol. 75, 5209–5217 (2009).
pubmed: 19542325
pmcid: 2725451
doi: 10.1128/AEM.00888-09
Wilson, J. J. & Kappler, U. Sulfite oxidation in Sinorhizobium meliloti. Biochim. Biophys. Acta 1787, 1516–1525 (2009).
pubmed: 19632192
doi: 10.1016/j.bbabio.2009.07.005
Lenk, S. et al. Novel groups of gammaproteobacteria catalyse sulfur oxidation and carbon fixation in a coastal, intertidal sediment. Environ. Microbiol. 13, 758–774 (2011).
pubmed: 21134098
doi: 10.1111/j.1462-2920.2010.02380.x
Wasmund, K., Mußmann, M. & Loy, A. The life sulfuric: Microbial ecology of sulfur cycling in marine sediments. Environ. Microbiol. Rep. 9, 323–344 (2017).
pubmed: 28419734
doi: 10.1111/1758-2229.12538
Crichton, R. Molybdenum, tungsten, vanadium and chromium. In Biological Inorganic Chemistry (ed. Crichton, R.) (Elsevier, UK, 2019).
Dahl, T. W., Chappaz, A., Fitts, J. P. & Lyons, T. W. Molybdenum reduction in a sulfidic lake: Evidence from x-ray absorption fine structure spectroscopy and implications for the Mo paleoproxy. Geochim. Cosmochim. Acta 103, 213–231 (2013).
doi: 10.1016/j.gca.2012.10.058
Nair, R. R., Silveira, C. M. & Diniz, M. S. Changes in metabolic pathways of desulfovibrio alaskensis G20 cells induced by molybdate excess. J. Biol. Inorg. Chem. 20, 311–322 (2015).
pubmed: 25488518
doi: 10.1007/s00775-014-1224-4
Bellenger, J., Arnaud-Neu, F. & Asfari, Z. Complexation of oxoanions and cationic metals by the biscatecholate siderophore azotochelin. J. Biol. Inorg. Chem. 12, 367–376 (2007).
pubmed: 17171370
doi: 10.1007/s00775-006-0194-6
Dahl, T. W. et al. Evidence of molybdenum association with particulate organic matter under sulfidic conditions. Geobiology 15(2), 311–323 (2017).
pubmed: 27997756
doi: 10.1111/gbi.12220
Wagner, M., Chappaz, A. & Lyons, T. W. Molybdenum speciation and burial pathway in weakly sulfidic environments: Insights from XAFS. Geochim. Cosmochim. Acta 206, 18–29 (2017).
doi: 10.1016/j.gca.2017.02.018
Bao, P. et al. The role of sulfate- reducing prokaryotes in the coupling of element biogeochemical cycling. Sci. Total Environ. 613–614, 398–408 (2018).
pubmed: 28918271
doi: 10.1016/j.scitotenv.2017.09.062
Poulson-Brucker, R. L., McManus, J., Severmann, S. & Berelson, W. M. Molybdenum behavior during early diagenesis: Insights from Mo isotopes. Geochem. Geophys. Geosyst. https://doi.org/10.1029/2008GC002180 (2009).
doi: 10.1029/2008GC002180
Poulson-Brucker, R. L., McManus, J. & Poulton, S. W. Molybdenum isotope fractionations observed under anoxic experimental conditions. Geochem. J. 46, 201–209 (2012).
doi: 10.2343/geochemj.1.0167
Xu, N., Christodoulatos, C. & Braida, W. Adsorption of molybdate and tetrathiomolybdate onto pyrite and goethite: Effect of pH and competitive ions. Chemosphere 62, 1726–1735 (2006).
pubmed: 16084558
doi: 10.1016/j.chemosphere.2005.06.025
Mohajerin, T. J., Helz, G. R. & Johannesson, K. H. Tungstem-molybdenum fractionation in estuarine environment. Geochim. Cosmochim. Acta 177, 105–119 (2016).
doi: 10.1016/j.gca.2015.12.030
Poulton, S. W., Fralick, P. W. & Canfield, D. E. The transition to a sulphidic ocean, ~1.84 billion years ago. Nature 431, 173–177 (2004).
pubmed: 15356628
doi: 10.1038/nature02912
Rasmussen, B. et al. Deposition of 1.88-billion-year-old iron formations as a consequence of rapid crustal growth. Nature 484, 498–501 (2012).
pubmed: 22538613
doi: 10.1038/nature11021
Ishida, A., Hashizume, K. & Kakegawa, T. Microbial nitrogen cycle enhanced by continental input recorded in the gunflint formation. Geochem. Persp. Let. 4, 13–18 (2017).
doi: 10.7185/geochemlet.1729
Hemkemeyer, M., Schwalb, S. A., Heinze, S., Joergensen, R. G. & Wichern, F. Functions of elements in soil microorganisms. Microbiol. Res. 252, 126832 (2021).
pubmed: 34508963
doi: 10.1016/j.micres.2021.126832
Jordan, S. F., Zuilen, M. A., Rouilland, J., Martins, Z. & Lane, N. Prebiotic membrane structures mimic the morphology of alleged early traces of life on Earth. Commun. Earth Envion. https://doi.org/10.1038/s43247-024-01372-0 (2024).
doi: 10.1038/s43247-024-01372-0
Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Wilson, R. SIMS quantification in Si, GaAs, and diamond—An update. Int. J. Mass Spec. Ion Procs. 143, 43–49 (1995).
doi: 10.1016/0168-1176(94)04136-U