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Fossilized Iron Bacteria Reveal a Pathway to the Biological Origin of Banded Iron Formation

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Fossilized Iron Bacteria Reveal a Pathway to the Biological Origin of Banded Iron Formation ARTICLE Received 11 Mar 2013 | Accepted 23 May 2013 | Published 20 Jun 2013 DOI: 10.1038/ncomms3050 Fossilized iron bacteria reveal a pathway to the biological origin of banded iron formation Ernest Chi Fru1,2, Magnus Ivarsson1,2, Stephanos P. Kilias3, Stefan Bengtson1,2, Veneta Belivanova1, Federica Marone4, Danielle Fortin5, Curt Broman6 & Marco Stampanoni4,7 Debates on the formation of banded iron formations in ancient ferruginous oceans are dominated by a dichotomy between abiotic and biotic iron cycling. This is fuelled by diffi- culties in unravelling the exact processes involved in their formation. Here we provide fossil environmental evidence for anoxygenic photoferrotrophic deposition of analogue banded iron rocks in shallow marine waters associated with an Early Quaternary hydrothermal vent field on Milos Island, Greece. Trace metal, major and rare earth elemental compositions suggest that the deposited rocks closely resemble banded iron formations of Precambrian origin. Well-preserved microbial fossils in combination with chemical data imply that band formation was linked to periodic massive encrustation of anoxygenic phototrophic biofilms by iron oxyhydroxide alternating with abiotic silica precipitation. The data implicate cyclic anoxygenic photoferrotrophy and their fossilization mechanisms in the construction of microskeletal fabrics that result in the formation of characteristic banded iron formation bands of varying silica and iron oxide ratios. 1 Swedish Museum of Natural History, Department of Palaeobiology, Box 50007, 105 05 Stockholm, Sweden. 2 Nordic Centre for Earth Evolution (NordCEE), Box 50007, 105 05 Stockholm, Sweden. 3 Department of Economic Geology and Geochemistry, Faculty of Geology and Geoenvironment, National and Kapodistrian University of Athens, Panepistimiopolis, Zographou, 15784, Athens, Greece. 4 Swiss Light Source, Paul Scherrer Institute, CH-5232 Villigen, Switzerland. 5 Department of Earth Sciences, University of Ottawa, Ottawa, Ontario, Canada. 6 Department of Geological Sciences, Stockholm University, Stockholm, Sweden. 7 Institute for Biomedical Engineering, University and ETH Zu¨rich, CH-8092 Zu¨rich, Switzerland. Correspondence and requests for materials should be addressed to E.C.F. (e-mail: [email protected]). NATURE COMMUNICATIONS | 4:2050 | DOI: 10.1038/ncomms3050 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3050 t is generally believed that banded iron formations (BIFs), (Supplementary Fig. S2). Similar to Precambrian BIFs, silica/iron the bulk of which was formed in the late Archaean/ ratios in these rocks are inversely related (Fig. 3a), while a low IPalaeoproterozoic marine basins, occurred in stratified water range of TiO2,Al2O3 and K2O concentrations suggest little columns deep in the ocean and on continental shelf margins1–4. terrigenous sedimentary input17–19. Heavy rare earth element Soluble ferrous iron, supplied from mid-ocean ridges and (REE) enrichment occurs in both the ferruginous and siliceous hydrothermal vents, was oxidized by various processes to ferric components of the rock relative to light REE (Fig. 3b) and is iron and deposited in association with varying silica ratios as comparable to reported Precambrian BIF profiles17–19. Together BIFs1–4. But the mechanism that drove and sustained the massive with a pronounced positive Eu anomaly, these observations and sporadic deposition of BIFs throughout much of the hint at a hydrothermal origin of the deposits as opposed to Precambrian remains a mystery, despite decades of research. seawater-derived sediments that are often light REE-enriched The low Archaean oxygen levels (B10 À 5 of present-day relative to heavy rare earth elements18. Calculated Eu/Eu* and concentrations or even less5) are generally considered Ce/Ce* anomalies (North American Shale Composite (NASC) insufficient to have supported broad-scale BIF generation1,6. normalized) of B0.23 and B2.56, respectively, lie within the Instead, biotic, anoxygenic photoferrotrophic precipitation reported Precambrian BIF range, while Ce depletion in relation to 2 þ 17–19 according to the equation 4Fe þ CO2 þ 11H2O þ light- the other REEs supports anoxic depositional conditions . þ 6–14 [CH2O] þ 4Fe(OH)3 þ 8H has been proposed . With the Sedimentary Ce levels are generally expected to increase under exemption of proxies such as iron isotopes12,13, there exists no oxidizing conditions because, unlike most REEs, Ce3 þ is direct environmental evidence—neither in ancient nor in modern oxidized to Ce4 þ and coprecipitated in association with iron ecosystems—demonstrating how photoferrotrophs could have oxyhydro(oxides)17–19. Furthermore, the occurrence and accounted for vast-scale biological BIF deposition, including the preservation of MnO (Fig. 3c) in concentrations comparable to formation of their spectacular banded consistency. Mesoarchean Witwatersrand Supergroup BIFs19 supports a Cape Vani, located on the NW of Milos Island, in the Hellenic reduced sedimentary environment. (Aegean) Volcanic Arc, hosts an Early Quaternary shallow Cr in oceanic sediments has been mostly associated with a ferruginous marine microbial deposit that was supported by terrigenous origin, resulting from the dissolution of ultramafic chemical energy released from focused and diffused hydrothermal rocks and soils20,21. In oxygenated conditions, the released Cr3 þ vents15,16. Biogeochemical evidence indicates that this deposit is oxidized by Mn(III) and (IV) to stable Cr6 þ , which under occurred in a restricted shallow marine basin at the foot of an reducing conditions is transformed by microbial activity and andesite continental shelf, where calm waters resulted in water Fe2 þ to Cr3 þ and preserved in association with iron column stratification and the development of local anoxia15.We oxyhydro(oxides)20,21. Instead, we found that Cr3 þ was provide new biogeochemical data supporting this fact and consistently below the detection limit, a situation similar to the independently illustrate that these conditions resemble those low Cr3 þ concentrations reported for much of Archaean that supported the deposition of some Precambrian BIFs, with the Agloma-type BIFs deposited close to deep submarine volcanic iron sourced from seafloor hydrothermal vents and hotspots. arcs and spreading ridges21. After B2.5 Ga, superior-type BIF facies (near-shore continental shelf deposits) were reported to have experienced a sudden spike in Cr concentrations, which was Results linked to the clastic detrital input resulting from oxygen-driven Geology and geochemistry. The Cape Vani rocks (Fig. 1; see weathering of crustal rocks20,21. Our Cr data thus support the Supplementary Fig. S1 for a description of the geology of the field idea of low oxygen tension in the water column, where the Cape site) display remarkable BIF-like patterns (Fig. 2), including Vani marine deposits were formed, with low levels of continental alternating micrometric to millimetric iron oxide and silica bands crust detrital delivery into the basin. Adriatic sea Black sea Aegean sea Turkey reece G LEGEND Alluvium Crete Mediterranean sea Products of phreatic activity Cape vani 36°45’ Rhyolite (UPI) Lava domes Pyroclastics (LPI) Dome complexes and lava flows Pyroclastic rocks (UPo) Marine sedimentary rocks (UMi-LPo) 36°40’ Metamorphic basement (M) 2 km Main area of themal manifestations 24°20’ 24°30’ N Figure 1 | Location and geologic features of Cape Vani. Inset, satellite map showing the location of Milos Island (black circle on unbroken white line). Grey circle on unbroken white line indicates Santorini. Broken white line shows the Hellenic Trench, where the African plate is subducted under the Euroasian plate to give rise to the Hellenic (Aegean) Volcanic Arc (unbroken white line). UPI—upper Pleistocene; LPI—lower Pleistocene; UPo—upper Pliocene; LPo—lower Pliocene; UMi—upper Miocene; M—Mesozoic (16). 2 NATURE COMMUNICATIONS | 4:2050 | DOI: 10.1038/ncomms3050 | www.nature.com/naturecommunications & 2013 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3050 ARTICLE The haematite signal varied in the Cape Vani deposits as a No organic carbon signal was obtained by Raman function of silica concentrations whereas trace elemental spectroscopy—a BIF feature often attributed to remineralization compositions followed the same general trends, regardless of of organic matter to dissolved inorganic carbon through the silica to iron ratio (Fig. 3d), indicating that the rocks were respiration22. The largely low levels of whole-rock total carbon deposited under persistent/consistent biogeochemical conditions supports this hypothesis, whereas the close to zero total sulphur for extended periods. The high silica load particularly suggests an concentrations suggest a non-sulphidic depositional environment ocean saturated with hydrothermally derived amorphous silica, (Fig. 3c). Therefore, the Cape Vani deposit could be classified similar to the inferences made for Precambrian oceans from a as a cherty, low-carbon, haematite-rich BIF analogue, formed chemical analysis of BIFs1,17,18. under reducing conditions. The recorded low oxygen con- ab Not to scale Millimeter-thick Mn(-Fe) crust Thick- to thin-bedded parallel- and cross-stratified sandstone Well sorted thick-bedded, granule- to pebble-bearing sandstone Thick-bedded, pebble to cobble 1m conglomerate with Fe- and Ba-rich matrix Jasper-banded red/white chert
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