Cycles within cycles – The significance of temperature cycling, microbial Fe cycling and low-grade metamorphic nutrient immobilization for the genesis of banded iron formations

Abstract

Banded Iron Formations (BIFs), Fe- and Si-rich marine chemical sedimentary deposits which formed during the Archean and Paleoproterozoic (between 3.8 to 1.85 Ga), are the product of complex interplay between a suite of different key processes: environmental factors such as nutrient availability and temperature, microbial activity, diagenesis, and low-grade metamorphism. Major deposits formed during the Neoarchean and Paleoproterozoic eras are frequently used for reconstructing the paleoenvironment and yet, critical aspects of their genesis are highly debated. Even fundamental questions such as the nature of the primary precipitate and the mechanisms underlying its formation remain poorly constrained. One potential model for the deposition of Archean and early Paleoproterozoic BIFs suggests that they formed through the metabolic activity of anoxygenic photoautotrophic Fe(II)-oxidizing bacteria (photoferrotrophs). This microbial activity would have led to the formation of poorly soluble Fe(III) (oxyhydr)oxides, which co-precipitated to varying degrees with organic carbon (Corg), thus forming primary BIF sediments. Photoferrotrophic bacteria as agents of BIF deposition is currently supported by the interpretation of BIF P/Fe ratios, which is based on the empirical partitioning coefficients for phosphate (PO43-) adsorption onto primary Fe(III) (oxyhydr)oxides, ultimately suggesting a PO43--poor ocean during the Archean and early Paleoproterozoic. However, it is unknown how stable the association between PO43- and primary Fe(III) (oxyhydr)oxides would have been under metamorphic conditions relevant for thermally immature (sub-greenschist facies) BIFs. The stability of the PO43--Fe(III) mineral co-precipitate and potential metamorphic PO43- remobilization could have important implications for the interpretation of P/Fe ratios in BIFs and the proposed mechanism for BIF deposition. Additionally, it remains unresolved how variations in the activity of photoferrotrophs, in response to temperature fluctuations, and the transformation of primary biogenic Fe(III) minerals during microbial Fe cycling in an early ocean would have influenced the deposition of BIFs. A previous study suggested that temperature fluctuations may be responsible for the alternating deposition of Fe- and Si-rich layers in BIFs, and thus have created their characteristic banding, by influencing the metabolic activity of photoferrotrophs. While such a proposition is sensible, it remains unclear what would ultimately cause the separation between Si and Fe, especially given the high adsorption affinity of Si to freshly formed Fe(III) (oxyhydr)oxides. Furthermore, it is poorly constrained how cell-Fe(III) mineral aggregates formed by photoferrotrophs would have been altered during sedimentation. One process whose significance for BIF genesis is well documented is dissimilatory Fe(III) reduction (DIR). DIR is a microbial metabolism where heterotrophic bacteria couple Fe(III) reduction to Corg oxidation, utilizing substrates such as cell-Fe(III) mineral aggregates, resulting in the formation of secondary minerals such as magnetite and siderite, both of which are found in BIFs today. While both photoferrotrophy and DIR are individually well understood in the context of BIF genesis, it is unknown how, and to what extent, both metabolic processes would have already interacted in the water column and how this potential microbial Fe cycle would have influenced the (trans)formation of secondary Fe minerals as well as the properties of the minerals formed. In summary, the overall goal of this thesis was to identify factors and mechanisms influencing the initial deposition of BIFs and to determine how the interplay between different microbial metabolisms would have influenced the (mineralogical) (trans)formation of primary precipitates during BIF genesis. Specifically, this thesis aimed to (1) quantify the influence of low-grade metamorphism on the post-depositional remobilization of PO43- from primary Fe(III) (oxyhydr)oxides. (2) Verify the validity of a temperature-cycling model for creating the characteristic banding in BIFs and identify the mechanism(s) ultimately responsible for the separation of Fe and Si. (3) Determine the influence of repeated microbial Fe cycling occurring under conditions relevant for the ancient ocean (high Fe and Si concentrations) on the resulting secondary mineralogy. Specifically, the formation and preservation of minerals such as magnetite and siderite during dynamic, alternating redox cycles. In chapter one of this thesis we exposed PO43--loaded ferrihydrite synthesized in the presence of different Si concentrations (0 mM, 0.5 mM, and 1.6 mM) to low-grade metamorphic conditions (170°C, 1.2 kbar) for 14 days. Following 14 days of incubation we found that metamorphic mineral transformation was primarily driven by Corg reactivity: hematite was the main mineral product in the absence of Corg or when complex Corg was used as proxy for ancient biomass. By contrast, magnetite and vivianite were formed when highly reactive glucose was used. Metamorphic PO43- remobilization depended on the mineral transformation pathway and up to 10 mol.% PO43- was remobilized when hematite was formed. However, PO43- was effectively immobilized when magnetite and vivianite were present (<1.5 mol.% mobilization). Collectively our results suggest that, although Corg reactivity had a profound influence on the metamorphic mineral transformation pathway, the overall extent of metamorphic PO43--mobilization was minor. Therefore, BIFs likely record ancient seawater PO43- concentrations with high fidelity (reliable within 10%), thus supporting an PO43--starved ancient ocean. In the study conducted in chapter two we cultivated the marine photoferrotroph Rhodovulum iodosum under conditions relevant for the ancient ocean and exposed it to temperatures fluctuating between 26°C (warm periods) and 5°C (cold period). We could show that during warm periods R. iodosum was metabolically active, resulting in the precipitation of primary Fe(III) (oxyhydr)oxides. Conversely, its metabolic activity was reduced during cold periods, which instead triggered the abiotic precipitation of amorphous Si. This confirms that temperature fluctuations could have triggered the alternating deposition of Fe-rich and Si-rich layers in BIFs. Furthermore, the combined results of scanning electron microscopy (SEM) analyses, surface charge measurements and potentiometric titrations suggest that Corg co-precipitated with Fe(III) (oxyhydr)oxides was responsible for the separation of Fe and Si, either by occupying surface functional groups required for Si sorption or due to electrostatic repulsion due to negatively-charged carboxyl/phosphodiester groups. Finally, in chapter three we co-cultivated the marine photoferrotroph Chlorobium sp. N1 with a marine Fe(III)-reducing enrichment culture under conditions relevant for the ancient ocean. Our results show that photoferrotrophs and Fe(III)-reducing bacteria formed a highly dynamic microbial Fe redox cycle. Combined wet geochemical and SEM results suggest that Si and Corg were co-precipitated with freshly formed Fe(III) (oxyhydr)oxides during Fe(II) oxidation and released back into solution upon reductive dissolution of the Fe(III) minerals during microbial Fe(III) reduction. High concentrations of Si favored the formation of short-range ordered Fe(III) minerals like ferrihydrite while a mixed Fe(II)-bearing mineral phase, consisting of siderite and/or a Fe(II)-silicate, formed during Fe(III) reduction. No magnetite formation was observed over three consecutive microbial Fe cycles. Overall, our results imply that microbial Fe cycling would have been an important process in the ancient ocean water column, leading to the co-deposition of a ferrihydrite-Si composite and Fe(II) minerals in the initial BIF sediments. In summary, this PhD thesis better constrained the microbial processes that took place during the initial deposition of Neoarchean to early Paleoproterozoic-aged BIFs and provided further evidence of the crucial role microbes likely played during the initial formation of primary BIF sediments. Their metabolic activity (as modulated by the paleoenvironment) and the microbial Fe cycle created by the interplay between different Fe-metabolizing bacteria offer potential explanations for some of the characteristics of BIFs: (1) their banding, (2) the presence of minerals such as siderite and Fe(II)-silicates, and (3) the low amount of Corg preserved in BIFs. This PhD thesis highlights the complexity underlying the genesis of BIFs, which is best untangled by taking a multidisciplinary approach.