FATE OF ORGANIC COMPOUNDS DURING TRANSFORMATION OF
FERRIHYDRITE TO HEMATITE IN IRON FORMATIONS
The absence of organic compounds from Precambrian iron formations (IF) challenges the hypothesis of their biogenic origin. Here we address the fate of adsorbed organic compounds during transformation from ferrihydrite to hematite. We used binding energies obtined from DFS and desorption data (TGA) and show that the transformation of ferrihydrite to hematite (solid state route) releases glycerol. Our results highlight that organic compounds adsorbed at precursor ferrihydrite could be desorbed already during the process of IF sedimentation and diagenesis. Our data suggest that the absence of organic compounds in IF should not be used as evidence against their biogenic origin.
Traditionally, iron formations (IFs) have been classified as a chemical sediment but an increasing amount of evidence points toward an active role of microbes in their precipitation (Koehler et al., 2010). However , the lack of sufficient amount of organic compounds in IF, or their diagenetic or metamorphic derivatives, challenges the hypothesis of their biogenic origin.
Extracellular polymeric substances (EPS) can promote FeOx nucleation (Sand et al., 2019) and microbially formed FeOx are often found in close association with the EPS. When the EPS get encrusted with FeOx, the polymers are shed and new EPS are formed which prevent encrustation of the microbe itself (Phoenix et al., 2000; Chan et al., 2004). The FeOx-EPS would have settled through the water column and get deposited on the sea floor as IFs. Such mechanism of IF deposition implies an initial presence of a significant amount of organic compounds.
Photo by Alexandra Rouillard
Microbial breakdown of organic compounds in the largely anoxic Precambrian oceans would have been minor (Canfield, 1998), however, diagenesis and metamorphism would have promoted degradation of the organic compounds. In anoxic microenvironments siderite can be a main product of such degradation (Köhler et al., 2013) but siderite is only found in some IFs and in insufficient amounts to account for the missing organic mass.
Transformation of FeOx
Hematite is a major component of IFs found today (Konhauser et al., 2017), but initially the FeOx in the FeOx-polymer complexes were most likely composed of ferrihydrite (Chan et al., 2004). The transformation to hematite would have happened both before (Sun et al., 2015) and after deposition on the seabed.
Depending on the solution conditions, ferrihydrite to hematite transformation can involve lepidocrocite and goethite as intermediary phases, e.g., through Fe(II) catalysed transformation (Hansel et al., 2003), or it can be direct (Cudennec & Lecerf, 2006). Transformation involving intermediary phases is a dissolution-precipitation process (Schwertmann & Murad, 1983) implying that the interface between ferrihydrite and organic compounds is eliminated. In this scenario, organic compounds would have been liberated to solution where they could have been readsorbed to the newly formed phases or released in the water column and subsequently degraded. The direct transformation from ferrihydrite to hematite is a solid-state transition where atoms move only locally to occupy new structural positions (Cudennec & Lecerf, 2006), without the loss of interface with adsorbed complexes. Thus, the direct transformation of ferrihydrite to hematite is not necessarily accompanied by a removal of organic compounds.
However, the Gibbs free energy of binding (ΔGbu) between ferrihydrite and EPS is larger than between hematite and EPS (Sand et al., 2019) implying that the polymers were more likely to desorb from hematite than from ferrihydrite. In such a case, the absence of organic compounds in IFs cannot be an argument against their biogenic origin.
To better understand the fate of adsorbed organic compounds during direct transformation from ferrihydrite to hematite, we used dynamic force spectroscopy (DFS) to measure the energy of binding between hematite and representative organic functional groups represented found in EPS. Subsequently we identified the functional group least likely to desorb during transformation and made carried out transformation experiments where we used thermogravimetric analysis (TGA) to measure the loss of organic compounds during transformation.
Combining top down and bottom up approaches:
Bulk nucleation experiments
Bulk desorption experiments (TGA)
Dynamic force spectroscopy (DFS)
Schematics of the DFS: self assembled monolayers with carboxyl, hydroxyl and phosphate headgroups covalently bonded to a gold coated AFM tip (thiol functionalization).
In the transformation experiments, ferrihydrite and glycerol were mixed at room temperature and left to equilibrate overnight. One sample was then taken for TGA (equilibrated sample) and the rest was placed in the oven at 90 ºC until the transformation was complete (aged sample).
Idea and hypothesis development was under funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 663830 and the Welsh Government and Higher Education Funding Council for Wales through the Sêr Cymru National Research Network for Low Carbon, Energy and Environment.