Magnetotactic bacteria (MTB) are microorganisms that produce magnetic nanoparticles (magnetosomes) for navigation. These magnetosomes, primarily magnetite or greigite, are preserved in sediments as conventional magnetofossils, serving as valuable biomarkers for life and redox geochemistry. Giant magnetofossils (>1 µm), of unknown biological origin, are also found in sediments and have been linked to past environmental changes. While putative magnetofossils have been reported from older rocks, robust evidence for conventional magnetofossils only extends to the mid-Cretaceous, and giant magnetofossils were largely documented from Eocene hyperthermal events. The study aims to investigate the oldest robust record of both conventional and giant magnetofossils, specifically examining their abundance and morphology across the Cenomanian-Turonian boundary and OAE2, a major carbon cycle perturbation. Understanding magnetofossil distribution throughout Earth's history is critical for reconstructing past iron cycles and their relationship with climatic events, such as OAEs. The Holland Park core, Virginia, offers a unique opportunity to address this due to its well-preserved sediments spanning this crucial time period.

Previous research has established the use of magnetofossils as proxies for past environmental conditions. While the existence of magnetotactic bacteria has been known for some time, the fossil record has lagged behind, with irrefutable evidence for conventional magnetofossils dating only to the mid-Cretaceous. Studies have suggested the existence of much older magnetofossils, but these lack the necessary combination of morphological, crystallographic, and magnetic data for definitive identification. Giant magnetofossils, a more recent discovery, have initially been associated with hyperthermal events, particularly the Paleocene-Eocene Thermal Maximum (PETM). However, recent work has expanded the known distribution of these fossils to more recent periods, including global cooling events, highlighting the need for a more comprehensive understanding of their ecological significance and distribution across the geologic record. The role of both MTB and GIBO in the marine iron cycle has been suggested, with iron limitation potentially influencing their abundance and distribution.

The study utilized a core sample from Holland Park, Virginia, spanning the Cenomanian-Turonian boundary and OAE2. Biostratigraphic analysis using calcareous nannofossils confirmed the age and stratigraphic position of the sediments. Total organic carbon (TOC) content and stable carbon isotopes (δ¹³Corg) were measured to characterize the organic matter and identify the OAE2 interval. Bulk magnetic measurements (saturation magnetization (Ms), saturation remanence (Mr), coercivity (Bc), and coercivity of remanence (Bcr)) were performed to assess magnetic grain size variations. First-order reversal curve (FORC) diagrams were generated from selected samples to identify magnetic signatures consistent with single-domain biogenic magnetite. Eight stratigraphic horizons were selected for electron microscopy analysis to identify and quantify conventional and giant magnetofossils. Magnetic extracts were prepared using a modified protocol, and both scanning electron microscopy (SEM) and transmission electron microscopy (TEM) were employed to image and analyze magnetofossils. Energy dispersive X-ray spectroscopy (EDS) and selected area electron diffraction (SAED) were used to determine the mineralogy of the particles. Detailed morphometric analyses were conducted to characterize the size and shape of both conventional and giant magnetofossils, focusing on identifying and describing potentially novel morphologies. Magnetofossil abundances and relative abundances of different morphologies were quantified for pre- and post-OAE2 intervals to assess changes in community structure.

The Holland Park core revealed abundant and morphologically diverse magnetofossils, including both conventional and giant forms, spanning the Cenomanian-Turonian boundary and OAE2. The FORC analysis confirmed the presence of single-domain biogenic magnetite in the sediments bookending OAE2. SEM and TEM imaging revealed a range of known conventional magnetofossil morphologies (cuboctahedra, bullets, prisms) and giant magnetofossil morphologies (bullets, spindles, needles, spearheads). Three potentially new giant magnetofossil morphologies were identified and named: seeds, squash, and spades. A significant decrease (~80%) in total conventional magnetofossil abundance was observed after OAE2, while giant magnetofossil abundance remained relatively constant. However, the percentage of magnetite volume attributed to giant magnetofossils increased substantially after OAE2, due to the significant reduction in conventional forms. The relative abundance of conventional cuboctahedral magnetofossils decreased after OAE2, while that of bullet-shaped magnetofossils increased. Changes in relative abundances of giant magnetofossil morphologies were also observed between the pre- and post-OAE2 intervals, with a notable decrease in giant bullets and an increase in spindles, needles, seeds, squash, and spades after OAE2. Dimensional analyses of giant magnetofossils indicated that Cretaceous forms fall within the same size range as those from the Paleocene and Eocene. The presence of a film on magnetic extracts from the post-OAE2 sediments suggests a potential difference in preservation between pre- and post-OAE2 intervals, with conventional magnetofossils appearing less well-preserved.

The findings demonstrate the oldest robust record of both conventional and giant magnetofossils. The substantial decrease in conventional magnetofossils after OAE2, coupled with the relatively unchanged abundance of giant magnetofossils, indicates different responses to environmental changes or diagenetic processes. The changes in relative abundance of specific magnetofossil morphologies, both conventional and giant, may reflect shifts in ecological conditions, such as water column stratification and nutrient availability. The consistency in giant magnetofossil morphologies across different time periods (Cretaceous, Paleocene, Eocene) suggests similar ecological niches and preferences for the organisms producing these fossils. The discovery of potentially new giant magnetofossil morphologies highlights the diversity of giant iron-biomineralizing organisms (GIBO) and their potential roles in past ecosystems. The observed differences in preservation between conventional and giant magnetofossils may reflect differences in their resistance to diagenetic alteration, with giant magnetofossils potentially better preserved due to their size. However, it also highlights the potential for bias in magnetofossil preservation studies. Further research is necessary to confirm the biogenicity of the newly described morphologies through additional crystallographic, micromagnetic modeling, and isotopic analysis.

This study presents the oldest robust record of both conventional and giant magnetofossils, extending the known range of these important biomarkers. The significant changes in magnetofossil abundance and morphology across the Cenomanian-Turonian boundary and OAE2 highlight the sensitivity of these organisms to environmental changes and provide insights into the ecological dynamics of both MTB and GIBO. The discovery of new giant magnetofossil morphologies underscores the diversity of iron-biomineralizing organisms and the need for further research into their evolutionary history and ecological roles. Future studies should focus on more detailed comparative analyses of giant magnetofossil assemblages from various well-documented sediment archives to improve our understanding of the environmental factors driving their morphological diversity and distribution.

The study is limited by the single core location. While the Holland Park core provides valuable data, extending the analysis to additional geographically diverse cores would strengthen the conclusions regarding the widespread distribution of giant magnetofossils and the generality of the observed changes in magnetofossil assemblages across the Cenomanian-Turonian boundary and OAE2. Further investigation is needed to fully confirm the biogenicity of the newly identified giant magnetofossil morphologies using additional techniques such as isotopic analyses. The interpretation of changes in magnetofossil abundances could be influenced by diagenetic processes, which cannot be entirely ruled out, although the authors argue that such processes would likely affect all morphologies similarly within each interval. The exact mechanisms behind the observed changes in magnetofossil abundance and morphology remain to be fully elucidated, requiring further research.