Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae.
Biological Evolution
Chlorophyll
/ chemistry
Chlorophyta
/ anatomy & histology
Coordination Complexes
/ chemistry
Democratic Republic of the Congo
Ecosystem
Eukaryotic Cells
Fossils
Geologic Sediments
/ analysis
History, Ancient
Microscopy, Electron, Transmission
Nickel
/ chemistry
Photosynthesis
/ physiology
Phylogeny
Plant Cells
/ physiology
Tetrapyrroles
/ chemistry
X-Ray Absorption Spectroscopy
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
10 01 2022
10 01 2022
Historique:
received:
21
05
2021
accepted:
03
12
2021
entrez:
11
1
2022
pubmed:
12
1
2022
medline:
27
1
2022
Statut:
epublish
Résumé
The acquisition of photosynthesis is a fundamental step in the evolution of eukaryotes. However, few phototrophic organisms are unambiguously recognized in the Precambrian record. The in situ detection of metabolic byproducts in individual microfossils is the key for the direct identification of their metabolisms. Here, we report a new integrative methodology using synchrotron-based X-ray fluorescence and absorption. We evidence bound nickel-geoporphyrins moieties in low-grade metamorphic rocks, preserved in situ within cells of a ~1 Gyr-old multicellular eukaryote, Arctacellularia tetragonala. We identify these moieties as chlorophyll derivatives, indicating that A. tetragonala was a phototrophic eukaryote, one of the first unambiguous algae. This new approach, applicable to overmature rocks, creates a strong new proxy to understand the evolution of phototrophy and diversification of early ecosystems.
Identifiants
pubmed: 35013306
doi: 10.1038/s41467-021-27810-7
pii: 10.1038/s41467-021-27810-7
pmc: PMC8748435
doi:
Substances chimiques
Coordination Complexes
0
Tetrapyrroles
0
Chlorophyll
1406-65-1
Nickel
7OV03QG267
Types de publication
Historical Article
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
146Informations de copyright
© 2022. The Author(s).
Références
Leavitt, P. R. A review of factors that regulate carotenoid and chlorophyll deposition and fossil pigment abundance. J. Paleolimnol. 9, 109–127 (1993).
doi: 10.1007/BF00677513
Gueneli, N. et al. 1.1-Billion-year-old porphyrins establish a marine ecosystem dominated by bacterial primary producers. Proc. Natl Acad. Sci. USA 115, E6978–E6986 (2018).
pubmed: 29987033
pmcid: 6064987
doi: 10.1073/pnas.1803866115
French, K. L. et al. Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc. Natl Acad. Sci. USA 112, 5915–5920 (2015).
pubmed: 25918387
pmcid: 4434754
doi: 10.1073/pnas.1419563112
Vinnichenko, G., Jarrett, A. J. M., Hope, J. M. & Brocks, J. J. Discovery of the oldest known biomarkers provides evidence for phototrophic bacteria in the 1.73 Ga Wollogorang Formation, Australia. Geobiology 18, 544–559 (2020).
pubmed: 32216165
doi: 10.1111/gbi.12390
François, C. et al. Contributions of U-Th-Pb dating on the diagenesis and sediment sources of the lower group (BI) of the Mbuji-Mayi Supergroup (Democratic Republic of Congo). Precambrian Res. 298, 202–219 (2017).
doi: 10.1016/j.precamres.2017.06.012
Baludikay, B. K. et al. Raman microspectroscopy, bitumen reflectance and illite crystallinity scale: comparison of different geothermometry methods on fossiliferous Proterozoic sedimentary basins (DR Congo, Mauritania and Australia. Int. J. Coal Geol. 191, 80–94 (2018).
Baludikay, B. K., Storme, J. Y., François, C., Baudet, D. & Javaux, E. J. A diverse and exquisitely preserved organic-walled microfossil assemblage from the Meso-Neoproterozoic Mbuji-Mayi Supergroup (Democratic Republic of Congo) and implications for Proterozoic biostratigraphy. Precambrian Res. 281, 166–184 (2016).
doi: 10.1016/j.precamres.2016.05.017
Pang, K. et al. The nature and origin of nucleus-like intracellular inclusions in Paleoproterozoic eukaryote microfossils. Geobiology 11, 499–510 (2013).
pubmed: 24033870
Adam, Z. R., Skidmore, M. L., Mogk, D. W. & Butterfield, N. J. A Laurentian record of the earliest fossil eukaryotes. Geology 45, 387–390 (2017).
doi: 10.1130/G38749.1
Tang, Q. et al. Organic-walled microfossils from the early Neoproterozoic Liulaobei Formation in the Huainan region of North China and their biostratigraphic significance. Precambrian Res. 236, 157–181 (2013).
doi: 10.1016/j.precamres.2013.07.019
Krings, M. Stigonema (Nostocales, Cyanobacteria) in the Rhynie chert (Lower Devonian, Scotland). Rev. Palaeobot. Palynol. 295, 104505 (2021).
doi: 10.1016/j.revpalbo.2021.104505
Agić, H., Moczydłowska, M. & Yin, L. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton – A window into the early eukaryote evolution. Precambrian Res. 297, 101–130 (2017).
doi: 10.1016/j.precamres.2017.04.042
Beghin, J. et al. Microfossils from the late Mesoproterozoic – early Neoproterozoic Atar/El Mreïti Group, Taoudeni Basin, Mauritania, northwestern Africa. Precambrian Res. 291, 63–82 (2017).
doi: 10.1016/j.precamres.2017.01.009
Butterfield, N. J., Knoll, A. H. & Sweet, K. Paleobiology of the Neoproterowic Svanbergfjellet formation, Spitsbergen. Foss. Strat. 34, (1994).
Leiming, Y., Xunlai, Y., Fanwei, M. & Jie, H. Protists of the upper Mesoproterozoic Ruyang Group in Shanxi Province, China. Precambrian Res. 141, 49–66 (2005).
doi: 10.1016/j.precamres.2005.08.001
Loron, C. & Moczydłowska, M. Tonian (Neoproterozoic) eukaryotic and prokaryotic organic-walled microfossils from the upper Visingsö Group, Sweden. Palynology 6122, 1–35 (2017).
Grey, K., Walter, M. R. & Calver, C. R. Neoproterozoic biotic diversification: snowball Earth or aftermath of the Acraman impact? Geology 31, 459–462 (2003).
doi: 10.1130/0091-7613(2003)031<0459:NBDSEO>2.0.CO;2
Nowak, H. et al. Filamentous eukaryotic algae with a possible Cladophoralean affinity from the Middle Ordovician Winneshiek Lagerstätte in Iowa, USA. Geobios 50, 303–309 (2017).
doi: 10.1016/j.geobios.2017.06.005
Prasad, B., Uniyal, S. N. & Asher, R. Organic-walled microfossils from the Proterozoic Vindhyan Supergroup of Son Valley, Madhya Pradesh, India. Palaeobotanist 54, 13–60 (2005).
Barghoorn, E. S. & Schopf, J. W. Microorganisms from the Late Precambrian of Central Australia. Science 150, 337–339 (1965).
pubmed: 17742361
doi: 10.1126/science.150.3694.337
Carlisle, E. M., Jobbins, M., Pankhania, V., Cunningham, J. A. & Donoghue, P. C. J. Experimental taphonomy of organelles and the fossil record of early eukaryote evolution. Sci. Adv. 7, 1–9 (2021).
doi: 10.1126/sciadv.abe9487
Sun, W. et al. Nucleus preservation in early Ediacaran Weng’an embryo-like fossils, experimental taphonomy of nuclei and implications for reading the eukaryote fossil record: Taphonomy and preservation of nuclei. Interface Focus 10, 20200015 (2020).
pubmed: 32637068
pmcid: 7333911
doi: 10.1098/rsfs.2020.0015
Butterfield, N. J. A Vaucheriacean alga from the middle Neoproterozoic of Spitsbergen: implications for the evolution of proterozoic eukaryotes and the Cambrian explosion. Paleobiology 30, 231–252 (2004).
doi: 10.1666/0094-8373(2004)030<0231:AVAFTM>2.0.CO;2
Hofmann, H. J. & Jackson, G. D. Shale-facies microfossils from the proterozoic Bylot Supergroup, Baffin Island, Canada. J. Paleontol. 68, 1–35 (1994).
doi: 10.1017/S0022336000062314
Hermann, T. N. & Podkovyrov, V. N. On the nature of the Precambrian microfossils Arctacellularia and Glomovertella. Paleontol. J. 42, 655–664 (2008).
doi: 10.1134/S0031030108060117
Javaux, E. J., Knoll, A. H. & Walter, M. Recognizing and interpreting the fossils of early eukaryotes. Orig. Life Evol. Biosph. 33, 75–94 (2003).
pubmed: 12967274
doi: 10.1023/A:1023992712071
Javaux, E. J., Knoll, A. H. & Walter, M. R. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2, 121–132 (2004).
doi: 10.1111/j.1472-4677.2004.00027.x
Butterfield, N. J. Oxygen, animals and oceanic ventilation: An alternative view. Geobiology 7, 1–7 (2009).
pubmed: 19200141
doi: 10.1111/j.1472-4669.2009.00188.x
Komárek, J. in Süßwasserflora von Mitteleuropa (eds. Büdel, B., Gärtner, G., Krienitz, L. & Schagerl, M.) 1–1130 (Springer Spektrum, 2013).
Graham, L. E. & Wilcox, L. W. Algae (Prentice Hall, 2000).
Premaor, E., Saxena, R. K., Souza, P. Ade & Kalkreuth, W. Fungal spores and fruiting bodies from Miocene deposits of the Pelotas Basin. Braz. Rev. Micropaleontol. 61, 255–270 (2018).
doi: 10.1016/j.revmic.2018.08.002
Taylor, T. N., Krings, M. & Taylor, E. L. Fossil Fungi (Academic Press, 2015).
Gladyshev, V. N. & Zhang, Y. Metallomics and the Cell (Springer, 2013).
Lewan, M. D. & Maynard, J. B. Factors controlling enrichment of vanadium and nickel in the bitumen of organic sedimentary rocks. Geochim. Cosmochim. Acta 46, 2547–2560 (1982).
doi: 10.1016/0016-7037(82)90377-5
Algeo, T. J. & Maynard, J. B. Trace-element behavior and redox facies in core shales of Upper Pennsylvanian Kansas-type cyclothems. Chem. Geol. 206, 289–318 (2004).
doi: 10.1016/j.chemgeo.2003.12.009
Baludikay, B. K. Biostratigraphie, paléoécologie et évolution thermique du Supergroupe Mésoprotérozoïque de Mbuji-Mayi, RdCongo. PhD thesis, Université de Liège. (2018).
Baker, E. W. & Louda, J. W. in Biological Markers in the Sedimentary Record (ed. Johns, R. B.) (Elsevier, 1986).
Verne-Mismer, J., Ocampo, R., Callot, H. J. & Albrecht, P. New chlorophyll fossils from moroccan oil shales. Porphyrins derived from chlorophyll C3 or a related pigment? Tetrahedron Lett. 31, 1751–1754 (1990).
doi: 10.1016/S0040-4039(00)88872-3
Nesbitt, J. A., Robertson, J. M., Swerhone, L. A. & Lindsay, M. B. J. Nickel geochemistry of oil sands fluid petroleum coke deposits, Alberta, Canada. Facets 3, 469–486 (2018).
doi: 10.1139/facets-2017-0115
Jiang, K. et al. Isolated Ni single atoms in graphene nanosheets for high-performance CO
doi: 10.1039/C7EE03245E
Xia, K., Bleam, W. & Helmke, P. A. Studies of the nature of binding sites of first row transition elements bound to aquatic and soil humic substances using X-ray absorption spectroscopy. Geochim. Cosmochim. Acta 61, 2223–2235 (1997).
doi: 10.1016/S0016-7037(97)00080-X
Schuth, N. et al. Biomimetic mono- and dinuclear Ni(I) and Ni(II) complexes studied by X-ray absorption and emission spectroscopy and quantum chemical calculations. J. Phys. Conf. Ser. 712, 8–12 (2016).
doi: 10.1088/1742-6596/712/1/012134
Nesbitt, J. A., Lindsay, M. B. J. J. & Chen, N. Geochemical characteristics of oil sands fluid petroleum coke. Appl. Geochem. 76, 148–158 (2017).
doi: 10.1016/j.apgeochem.2016.11.023
Lytle, F. W. Cold Lake Asphaltene V. and Ni X. A. S. Spectra. International X-ray Absorption Society XAFS Database. (1983).
Delpomdor, F., Bonneville, S., Baert, K. & Préat, A. An introduction to the Precambrian petroleum system in the Sankuru-Mbuji-Mayi-Lomami-Lovoy Basin, South-Central Democratic Republic of Congo. J. Pet. Geol. 41, 5–27 (2018).
doi: 10.1111/jpg.12690
Rasmussen, B., Muhling, J. R. & Fischer, W. W. Ancient oil as a source of Carbonaceous matter in 1.88-billion-year-old gunflint stromatolites and microfossils. Astrobiology 21, 655–672 (2021).
pubmed: 33684328
doi: 10.1089/ast.2020.2376
Callot, H. J., Ocampo, R. & Albrecht, P. Sedimentary porphyrins: correlations with biological precursors. Energy Fuels 4, 635–639 (1990).
doi: 10.1021/ef00024a002
Cihlář, J., Füssy, Z. & Oborník, M. in Advances in Botanical Research (ed. Grimm, B.) (Academic Press, 2019).
Gledhill, M. The determination of heme b in marine phyto- and bacterioplankton. Mar. Chem. 103, 393–403 (2007).
doi: 10.1016/j.marchem.2006.10.008
Xu, Y., Ibrahim, I. M. & Harvey, P. J. The influence of photoperiod and light intensity on the growth and photosynthesis of Dunaliella salina (chlorophyta) CCAP 19/30. Plant Physiol. Biochem. 106, 305–315 (2016).
pubmed: 27231875
pmcid: 5250801
doi: 10.1016/j.plaphy.2016.05.021
Ferreira, V. S., Pinto, R. F. & Sant’Anna, C. Low light intensity and nitrogen starvation modulate the chlorophyll content of Scenedesmus dimorphus. J. Appl. Microbiol. 120, 661–670 (2016).
pubmed: 26598940
doi: 10.1111/jam.13007
Hanna, D. A. et al. Heme bioavailability and signaling in response to stress in yeast cells. J. Biol. Chem. 293, 12378–12393 (2018).
pubmed: 29921585
pmcid: 6093230
doi: 10.1074/jbc.RA118.002125
Hanna, D. A., Martinez-Guzman, O. & Reddi, A. R. Heme gazing: illuminating eukaryotic heme trafficking, dynamics, and signaling with fluorescent heme sensors. Biochemistry 56, 1815–1823 (2017).
pubmed: 28316240
doi: 10.1021/acs.biochem.7b00007
Donegan, R. K., Moore, C. M., Hanna, D. A. & Reddi, A. R. Handling heme: the mechanisms underlying the movement of heme within and between cells. Free Radic. Biol. Med. 133, 88–100 (2019).
pubmed: 30092350
doi: 10.1016/j.freeradbiomed.2018.08.005
Butterfield, N. J. Early evolution of the Eukaryota. Palaeontology 58, 5–17 (2015).
doi: 10.1111/pala.12139
Gibson, T. M. et al. Precise age of Bangiomorpha pubescens dates the origin of eukaryotic photosynthesis. Geology 46, 135–138 (2018).
doi: 10.1130/G39829.1
Tang, Q., Pang, K., Yuan, X. & Xiao, S. A one-billion-year-old multicellular chlorophyte. Nat. Ecol. Evol. 4, 543–549 (2020).
pubmed: 32094536
pmcid: 8668152
doi: 10.1038/s41559-020-1122-9
Parfrey, L. W., Lahr, D. J. G., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).
pubmed: 21810989
pmcid: 3158185
doi: 10.1073/pnas.1110633108
Yang, E. C. et al. Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Sci. Rep. 6, 1–11 (2016).
Sánchez-Baracaldo, P., Raven, J. A., Pisani, D. & Knoll, A. H. Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc. Natl. Acad. Sci. USA 114, E7737–E7745 (2017).
Grey, K. A modified palynological preparation technique for the extraction of large Neoproterozoic acanthomorph acritarchs and other acid insoluble microfossils. (Geological Survey of Western Australia, 1999).
Sforna, M. C. et al. Patterns of metal distribution in hypersaline microbialites during early diagenesis: implications for the fossil record. Geobiology 15, 259–279 (2017).
pubmed: 27935656
doi: 10.1111/gbi.12218
Ravel, B. & Newville, M. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12, 537–541 (2005).
pubmed: 15968136
doi: 10.1107/S0909049505012719
Schopf, J. W. in The Proterozoic Biosphere (eds. Schopf, J. W. & Klein, C.) (Cambridge Univ. Press, 1992).