Influence of Microbial Biofilms on the Preservation of Primary Soft Tissue in Fossil and Extant Archosaurs

Abstract

BackgroundMineralized and permineralized bone is the most common form of fossilization in the vertebrate record. Preservation of gross soft tissues is extremely rare, but recent studies have suggested that primary soft tissues and biomolecules are more commonly preserved within preserved bones than had been presumed. Some of these claims have been challenged, with presentation of evidence suggesting that some of the structures are microbial artifacts, not primary soft tissues. The identification of biomolecules in fossil vertebrate extracts from a specimen of Brachylophosaurus canadensis has shown the interpretation of preserved organic remains as microbial biofilm to be highly unlikely. These discussions also propose a variety of potential mechanisms that would permit the preservation of soft-tissues in vertebrate fossils over geologic time.Methodology/Principal FindingsThis study experimentally examines the role of microbial biofilms in soft-tissue preservation in vertebrate fossils by quantitatively establishing the growth and morphology of biofilms on extant archosaur bone. These results are microscopically and morphologically compared with soft-tissue extracts from vertebrate fossils from the Hell Creek Formation of southeastern Montana (Latest Maastrichtian) in order to investigate the potential role of microbial biofilms on the preservation of fossil bone and bound organic matter in a variety of taphonomic settings. Based on these analyses, we highlight a mechanism whereby this bound organic matter may be preserved.Conclusions/SignificanceResults of the study indicate that the crystallization of microbial biofilms on decomposing organic matter within vertebrate bone in early taphonomic stages may contribute to the preservation of primary soft tissues deeper in the bone structure.

Role of Sediment Size and Biostratinomy on the Development of Biofilms in Recent Avian Vertebrate Remains

“…In order to quantify the degree of modern biofilm infiltration in extant theropod bone, natural osteological vectors were identified on the surface of SEM samples at a magnification of 300×. Following Peterson et al (2010), a series of four nominal classes were established to categorize the degree of biofilm infiltration (Table 2; Figures 4A-D). A natural vector with no visible biofilm was classified as Class 0 (Figure 4A), a vector with a thin biofilm coating the inner wall of the canal was classified as Class 1 (Figure 4B), a Class 2 vector exhibits thickening biofilm that is beginning to close the aperture of the pore aperture of the vector (Figure 4C), and a Class 3 vector possesses a nearly complete infilling of the canal by biofilm (Figure 4D).…”

“…The water flowed through a variety of sediments with textures representative of common fluvial settings containing extant theropod bones, which were then analyzed for degree of biofilm formation, defined as a series of Classes (after Peterson et al, 2010). To appropriately model the taphonomy of fossil theropod specimens previously reported to possess primary soft-tissues that may be influenced by biofilms, such as subadult tyrannosaurs (Peterson et al, 2010), eight femora of the extant theropod Gallus gallus domesticus (Domestic Chicken) were selected and carefully stripped of bulk muscle and connective tissues with a sterilized scalpel. Samples were obtained from commercial sources (i.e., organic grocery stores in Northern Illinois).…”

“…Particles of aggregated hematite have been suggested to play a role in the preservation of collagen in such fossils (Schweitzer et al, 2005(Schweitzer et al, , 2016; Lee et al, 2017). Crucially, growth of microbial biofilms, prokaryotic organisms in an exopolymeric matrix (Schweitzer et al, 2016), on the surface of bone and the subsequent sealing of natural osteological vectors like pores of blood vessels and Haversian and Volkmann's canals have been suggested to facilitate the preservational mechanisms that occur during the early phases of diagenesis; biofilm infiltration leads to mineralization, retarding further metabolization of organic materials and promoting soft tissue preservation (Trinajstic et al, 2007;Peterson et al, 2010;Schweitzer et al, 2016).…”

“…Some previous analyses of early diagenetic biofilm growth on archosaur bones used the Extant Phylogenetic Bracket (EPB) method of inference after Witmer (1995) to focus on the influence of higher order phylogenetic variation and biostratinomic processes (e.g., trampling and subsequent fracturing before burial) with extant analogs (Peterson et al, 2010). Crushing of a bioclast (biostratinomy), which can stem from particle transport in high-energy fluvial systems, diagenetic alteration, or macrovertebrate bioturbation, produces new vectors for microbial infiltration of bone pore spaces in the form of cracks and fractures, providing open conditions for decomposition of internal organic materials in bones.…”

“…Crushing of a bioclast (biostratinomy), which can stem from particle transport in high-energy fluvial systems, diagenetic alteration, or macrovertebrate bioturbation, produces new vectors for microbial infiltration of bone pore spaces in the form of cracks and fractures, providing open conditions for decomposition of internal organic materials in bones. Bone alteration, such as crushing and fracturing, has previously been illustrated to have a statistically significant impact on biofilm formation and infiltration (Peterson et al, 2010).…”