Pyrite (iron sulphide, FeS2, also known as “fool’s gold”) is a widespread mineral found in deep sea sediments [1], [2] and many rocks and minerals [2], [3]. This includes those enriched with kerogen, the insoluble organic deposit that can accompany and generate oil. Typical organic precursors of kerogen are algae and woody plants.
The origins of pyrite deposits vary, but one particularly noteworthy form of pyrite frequently encountered in rocks is referred to as “framboids”, due to the raspberry-like appearance of spherical clusters of approximately equiaxed submicron particles that can be either rounded or polygonal in shape. These pyrite arrangements may carry a coded message about the origins of their formation.
It has been proposed and discussed in the literature [2] that the confined and controlled space within the frustules of diatom algae offers a favourable environment for framboid formation. What has so far remained elusive is confirmation of whether the process of pyrite formation is a purely chemical, abiotic reaction of Fe2+ ions with H2S/HS− ions; or if alternatively it is a biotic process [4] that takes place at the surface of Gram positive and negative bacteria that exist in spherical colonies and are responsible for framboid production, and their observed morphology.
The magnetosomes of magnetotactic bacteria[5] that are believed to serve as nanometer nuclei (seeds) for the precipitation of submicron pyrite grains in framboids [2] contain the necessary amount of iron to support pyrite formation, while surrounding organic matter serves as the source of H2S. Local temperature and chemical conditions govern the shape of pyrite grains in framboids allowing to form a variety of exterior habits characteristic of cubic crystals [6].
A fascinating outstanding question concerns when and how magnetotactic bacteria colonize the interior space of diatom frustules to enable the growth of pyrite framboids, what local thermodynamic conditions prevail, and what serves as the sources of iron and sulphur – intra- or extracellular – that control the kinetics of framboid growth. Two mechanisms of diatom frustule bacterial colonization and pyrite formation may be surmised: (a) endosymbiotic bacteria that settle inside living diatoms, as was recently shown for siderophores [7], or (b) bacteria such as Desulfovibrionales that colonize frustules after diatom cell apoptosis.
Diatomite silica rocks formed in the Earth crust from ancient deep sea sediments frequently contain heavy, viscous crude oil [8] as well as pyrite in the form of framboids [9]. The direct evidence of morphological similarity between framboids found within diatoms, and those seen in mineral deposits provide a strong link to the prominent role played by diatoms in the occurrence of pyrite framboids in rock. The importance of pyrite in oily rocks is highlighted by the fact that at elevated temperature and pressure when silica rocks are formed from diatomaceous/radiolarian sediments, the presence of FeS2 pyrite catalyses the kerogen-to-oil transformation [10].
The cover image represents a typical example of intra-diatom framboids present in this case within the frustule of diatom Rhizosolenia antennata. The imaged diatom was found in benthos samples collected at Antarctic shores at 680?m depth in Prydz Bay, Cooperation Sea, in the area of Russian polar station Progress (69°22′25″S 76°22′18″E). The cores were collected from the deck of RV Akademik Fedorov research ship during the 2017–18 Russian Antarctic expedition. The corer of 0.25?m2 cross-sectional area was lowered to the seabed using steel line, and a plastic sample tube was sunk into the sea sediment to the depth of 15–20?mm. The lack of characteristic H2S odour from the withdrawn sample indicated aerobic conditions at probe site, suggesting the prevalence of endosymbiotic bacteria in framboid formation.
It is remarkable to observe the variety of diatom species seen in the background of the cover image that has been confirmed in our large area SEM imaging experiments. Diatom algae are photosynthesising, and capture carbon dioxide dissolved in sea water. The favourable conditions for diatom proliferation in the cold polar regions can perhaps be well described by the title of a book by Françoise Sagan, “Un peu de soleil dans l’eau froide”.
The significance of diatom algae in the oil formation process has been well documented, along with their prominent role in the global biomineralization during the present geological era. Deeper insights into the important stages of pyrite and kerogen formation via endosymbiotic bacteria route may be obtained through in vitro studies in bioreactors [11].
Nanostructured iron sulphide mineral pyrite particles have recently attracted strong attention as efficient materials for energy [12], charge storage [13] and photovoltaic [14] applications. Hence, aquaculture cultivation of diatom algae under appropriate carefully chosen conditions may open up new opportunities for nanobiotechnology [15] low-cost production of photovoltaic, energy storage, and optoelectronic devices.
Purposeful cultivation of symbiotic societies of diatoms and magnetotactic bacteria in bioreactors enhanced by rigorous control over media temperature and chemical composition, and external magnetic field may allow to guide the hierarchical framboid structure formation for novel nanostructured smart energy sources and provide a link to silicon electronics by localising diatoms at the surface of patterned wafer substrates [16].
Acknowledgements
The authors wish to express their gratitude for funding support provided through the Royal Society grant IEC/R2/170223, RFBR grant 18-33-20132, and UK EPSRC project EP/P005381/1.
Further reading
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[10] X. Ma, et al.
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[14] Y. Bi, Y. Yuan, C.L. Exstrom, S.A. Darveau, J. Huang
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[16] A.M. Korsunsky, et al.
Mater. Today, 22 (2019), p. 159