SIMS analyses of the oldest known assemblage of microfossils document their taxon-correlated carbon isotope compositions

Schopf, J. William; Kitajima, Kouki; Spicuzza, Michael J.; Kudryavtsev, Anatoliy B.; Valley, John W.

doi:10.1073/pnas.1718063115

SIMS analyses of the oldest known assemblage of microfossils document their taxon-correlated carbon isotope compositions

Journal Article · Mon Dec 18 00:00:00 EST 2017 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1718063115· OSTI ID:1661864

^[1]; Kitajima, Kouki ^[2]; Spicuzza, Michael J. ^[2]; Kudryavtsev, Anatoliy B. ^[3]; Valley, John W. ^[2]

Univ. of California, Los Angeles, CA (United States); Univ. of Wisconsin, Madison, WI (United States); UW-Madison
Univ. of Wisconsin, Madison, WI (United States)
Univ. of California, Los Angeles, CA (United States)

Analyses by secondary ion mass spectroscopy (SIMS) of 11 specimens of five taxa of prokaryotic filamentous kerogenous cellular microfossils permineralized in a petrographic thin section of the ~3,465 Ma Apex chert of northwestern Western Australia, prepared from the same rock sample from which this earliest known assemblage of cellular fossils was described more than two decades ago, show their δ13C compositions to vary systematically taxon to taxon from -31‰ to -39‰. These morphospecies-correlated carbon isotope compositions confirm the biogenicity of the Apex fossils and validate their morphology-based taxonomic assignments. Perhaps most significantly, the δ¹³C values of each of the five taxa are lower than those of bulk samples of Apex kerogen (-27‰), those of SIMS-measured fossil-associated dispersed particulate kerogen (-27.6‰), and those typical of modern prokaryotic phototrophs (-25 ± 10‰). The SIMS data for the two highest δ¹³C Apex taxa are consistent with those of extant phototrophic bacteria; those for a somewhat lower δ¹³C taxon, with nonbacterial methane-producing Archaea; and those for the two lowest δ¹³C taxa, with methane-metabolizing γ-proteobacteria. Although the existence of both methanogens and methanotrophs has been inferred from bulk analyses of the carbon isotopic compositions of pre-2,500 Ma kerogens, these in situ SIMS analyses of individual microfossils present data interpretable as evidencing the cellular preservation of such microorganisms and are consistent with the near-basal position of the Archaea in rRNA phylogenies.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-93ER14389

OSTI ID:: 1661864

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 1 Vol. 115; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (41)

A Comparison of the Filamentous iron Organisms, Clonothrix Fusca roze and Crenothrix Polyspora cohn Kolk, Laura A. American Journal of Botany, Vol. 25, Issue 1 https://doi.org/10.1002/j.1537-2197.1938.tb09180.x	journal	January 1938
Extraction and carbon isotope analysis of CO2 from scapolite in deep crustal granulites and xenoliths Moecher, David P.; Valley, John W.; Essene, Eric J. Geochimica et Cosmochimica Acta, Vol. 58, Issue 2 https://doi.org/10.1016/0016-7037(94)90518-5	journal	January 1994
Factors controlling 13C contents of sedimentary organic compounds: Principles and evidence Hayes, J. M. Marine Geology, Vol. 113, Issue 1-2 https://doi.org/10.1016/0025-3227(93)90153-M	journal	July 1993
Carbon isotopes and petrography of kerogens in ∼3.5-Ga hydrothermal silica dikes in the North Pole area, Western Australia Ueno, Yuichiro; Yoshioka, Hideyoshi; Maruyama, Shigenori Geochimica et Cosmochimica Acta, Vol. 68, Issue 3 https://doi.org/10.1016/S0016-7037(03)00462-9	journal	February 2004
Volcanic degassing, hydrothermal circulation and the flourishing of early life on Earth: A review of the evidence from c. 3490-3240 Ma rocks of the Pilbara Supergroup, Pilbara Craton, Western Australia Vankranendonk, M. Earth-Science Reviews, Vol. 74, Issue 3-4 https://doi.org/10.1016/j.earscirev.2005.09.005	journal	February 2006
Preservation and detection of microstructural and taxonomic correlations in the carbon isotopic compositions of individual Precambrian microfossils Williford, Kenneth H.; Ushikubo, Takayuki; Schopf, J. William Geochimica et Cosmochimica Acta, Vol. 104 https://doi.org/10.1016/j.gca.2012.11.005	journal	March 2013
Biogenicity of Earth's earliest fossils: A resolution of the controversy Schopf, J. William; Kudryavtsev, Anatoliy B. Gondwana Research, Vol. 22, Issue 3-4 https://doi.org/10.1016/j.gr.2012.07.003	journal	November 2012
Critical testing of Earth's oldest putative fossil assemblage from the ∼3.5Ga Apex chert, Chinaman Creek, Western Australia Brasier, M.; Green, O.; Lindsay, J. Precambrian Research, Vol. 140, Issue 1-2 https://doi.org/10.1016/j.precamres.2005.06.008	journal	October 2005
Microstructure-specific carbon isotopic signatures of organic matter from ∼3.5 Ga cherts of the Pilbara Craton support a biologic origin Morag, Navot; Williford, Kenneth H.; Kitajima, Kouki Precambrian Research, Vol. 275 https://doi.org/10.1016/j.precamres.2016.01.014	journal	April 2016
An anaerobic ∼3400 Ma shallow-water microbial consortium: Presumptive evidence of Earth’s Paleoarchean anoxic atmosphere Schopf, J. William; Kudryavtsev, Anatoliy B.; Osterhout, Jeffrey T. Precambrian Research, Vol. 299 https://doi.org/10.1016/j.precamres.2017.07.021	journal	September 2017
Methanotrophic bacteria occupy benthic microbial mats in shallow marine hydrocarbon seeps, Coal Oil Point, California: METHANOTROPHIC MICROBIAL MATS Ding, Haibing; Valentine, David L. Journal of Geophysical Research: Biogeosciences, Vol. 113, Issue G1 https://doi.org/10.1029/2007JG000537	journal	February 2008
Filamentous microfossils in a 3,235-million-year-old volcanogenic massive sulphide deposit Rasmussen, Birger Nature, Vol. 405, Issue 6787 https://doi.org/10.1038/35015063	journal	June 2000
Laser–Raman imagery of Earth's earliest fossils Schopf, J. William; Kudryavtsev, Anatoliy B.; Agresti, David G. Nature, Vol. 416, Issue 6876 https://doi.org/10.1038/416073a	journal	March 2002
Questioning the evidence for Earth's oldest fossils Brasier, Martin D.; Green, Owen R.; Jephcoat, Andrew P. Nature, Vol. 416, Issue 6876 https://doi.org/10.1038/416076a	journal	March 2002
Dating earliest life Moorbath, Stephen Nature, Vol. 434, Issue 7030 https://doi.org/10.1038/434155a	journal	March 2005
Haematite pseudomicrofossils present in the 3.5-billion-year-old Apex Chert Marshall, Craig P.; Emry, Julienne R.; Olcott Marshall, Alison Nature Geoscience, Vol. 4, Issue 4 https://doi.org/10.1038/ngeo1084	journal	February 2011
Hydrothermal alteration and microfossil artefacts of the 3,465-million-year-old Apex chert Pinti, Daniele L.; Mineau, Raymond; Clement, Valentin Nature Geoscience, Vol. 2, Issue 9 https://doi.org/10.1038/ngeo601	journal	August 2009
Cohn’s Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase Stoecker, Kilian; Bendinger, Bernd; Schöning, Björn Proceedings of the National Academy of Sciences, Vol. 103, Issue 7 https://doi.org/10.1073/pnas.0506361103	journal	February 2006
Changing the picture of Earth's earliest fossils (3.5–1.9 Ga) with new approaches and new discoveries Brasier, Martin D.; Antcliffe, Jonathan; Saunders, Martin Proceedings of the National Academy of Sciences, Vol. 112, Issue 16 https://doi.org/10.1073/pnas.1405338111	journal	April 2015
Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Woese, C. R.; Kandler, O.; Wheelis, M. L. Proceedings of the National Academy of Sciences, Vol. 87, Issue 12 https://doi.org/10.1073/pnas.87.12.4576	journal	June 1990
Carbon Isotopic Signatures of Individual Archean Microfossils(?) from Western Australia Ueno, Yuichiro; Isozaki, Yukio; Yurimoto, Hisayoshi International Geology Review, Vol. 43, Issue 3 https://doi.org/10.1080/00206810109465008	journal	March 2001
Morphology: An Ambiguous Indicator of Biogenicity García Ruiz, Juan Manuel; Carnerup, Anna; Christy, Andrew G. Astrobiology, Vol. 2, Issue 3 https://doi.org/10.1089/153110702762027925	journal	August 2002
Fossil evidence of Archaean life Schopf, J. William Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1470 https://doi.org/10.1098/rstb.2006.1834	journal	May 2006
Reclassification of the Crenarchaeal Orders and Families in Accordance with 16S rRNA Sequence Data Burggraf, S.; Huber, H.; Stetter, K. O. International Journal of Systematic Bacteriology, Vol. 47, Issue 3 https://doi.org/10.1099/00207713-47-3-657	journal	July 1997
Enrichment, Isolation and Some Properties of Methane-utilizing Bacteria Whittenbury, R.; Phillips, K. C.; Wilkinson, J. F. Journal of General Microbiology, Vol. 61, Issue 2 https://doi.org/10.1099/00221287-61-2-205	journal	May 1970
Review of the Pilbara Craton and Fortescue Basin, Western Australia: Crustal evolution providing environments for early life: Pilbara Craton and Fortescue Basin Hickman, Arthur Hugh Island Arc, Vol. 21, Issue 1 https://doi.org/10.1111/j.1440-1738.2011.00783.x	journal	February 2012
Self-Assembled Silica-Carbonate Structures and Detection of Ancient Microfossils Garcia-Ruiz, J. M. Science, Vol. 302, Issue 5648 https://doi.org/10.1126/science.1090163	journal	November 2003
Microfossils of the Early Archean Apex Chert: New Evidence of the Antiquity of Life Schopf, J. W. Science, Vol. 260, Issue 5108 https://doi.org/10.1126/science.260.5108.640	journal	April 1993
Atmospheric Influence of Earth's Earliest Sulfur Cycle Farquhar, J. Science, Vol. 289, Issue 5480 https://doi.org/10.1126/science.289.5480.756	journal	August 2000
Clonothrix fusca Roze 1896, a Filamentous, Sheathed, Methanotrophic γ-Proteobacterium Vigliotta, Giovanni; Nutricati, Eliana; Carata, Elisabetta Applied and Environmental Microbiology, Vol. 73, Issue 11 https://doi.org/10.1128/AEM.02678-06	journal	April 2007
Morphological Survey of Microbial Mats Near Deep-Sea Thermal Vents † Jannasch, Holger W.; Wirsen, Carl O. Applied and Environmental Microbiology, Vol. 41, Issue 2 https://doi.org/10.1128/AEM.41.2.528-538.1981	journal	January 1981
Bacterial evolution. Woese, C. R. Microbiological Reviews, Vol. 51, Issue 2 https://doi.org/10.1128/MMBR.51.2.221-271.1987	journal	January 1987
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/MMBR.60.2.439-471.1996	journal	January 1996
Morphological Survey of Microbial Mats Near Deep-Sea Thermal Vents † Jannasch, Holger W.; Wirsen, Carl O. Applied and Environmental Microbiology, Vol. 41, Issue 2 https://doi.org/10.1128/aem.41.2.528-538.1981	journal	January 1981
Bacterial evolution Woese, C. R. Microbiological Reviews, Vol. 51, Issue 2 https://doi.org/10.1128/mr.51.2.221-271.1987	journal	June 1987
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/mr.60.2.439-471.1996	journal	January 1996
Middle Archean volcano-hydrothermal sequence: Bacterial microfossil-bearing 3.2 Ga Dixon Island Formation, coastal Pilbara terrane, Australia Kiyokawa, S.; Ito, T.; Ikehara, M. Geological Society of America Bulletin, Vol. 118, Issue 1-2 https://doi.org/10.1130/B25748.1	journal	January 2006
Cyanobacteria associated with hot spring travertines Pentecost, Allan Canadian Journal of Earth Sciences, Vol. 40, Issue 11 https://doi.org/10.1139/e03-075	journal	November 2003
Complete genome sequence of and proposal of Thermofilum uzonense sp. nov. a novel hyperthermophilic crenarchaeon and emended description of the genus Thermofilum Toshchakov, Stepan V.; Korzhenkov, Aleksei A.; Samarov, Nazar I. Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0105-y	journal	December 2015
A Comparison of the Filamentous Iron Organisms, Clonothrix Fusca Roze and Crenothrix Polyspora Cohn Kolk, Laura A. American Journal of Botany, Vol. 25, Issue 1 https://doi.org/10.2307/2436625	journal	January 1938
Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 2. Isotopic constraints Alperin, M. J.; Hoehler, T. M. American Journal of Science, Vol. 309, Issue 10 https://doi.org/10.2475/10.2009.02	journal	December 2009

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