Microbially mediated fossil concretions and their characterization by the latest methodologies: a review

Abstract

The study of well-preserved organic matter (OM) within mineral concretions has provided key insights into depositional and environmental conditions in deep time. Concretions of varied compositions, including carbonate, phosphate, and iron-based minerals, have been found to host exceptionally preserved fossils. Organic geochemical characterization of concretion-encapsulated OM promises valuable new information of fossil preservation, paleoenvironments, and even direct taxonomic information to further illuminate the evolutionary dynamics of our planet and its biota. Full exploitation of this largely untapped geochemical archive, however, requires a sophisticated understanding of the prevalence, formation controls and OM sequestration properties of mineral concretions. Past research has led to the proposal of different models of concretion formation and OM preservation. Nevertheless, the formation mechanisms and controls on OM preservation in concretions remain poorly understood. Here we provide a detailed review of the main types of concretions and formation pathways with a focus on the role of microbes and their metabolic activities. In addition, we provide a comprehensive account of organic geochemical, and complimentary inorganic geochemical, morphological, microbial and paleontological, analytical methods, including recent advancements, relevant to the characterization of concretions and sequestered OM. The application and outcome of several early organic geochemical studies of concretion-impregnated OM are included to demonstrate how this underexploited geo-biological record can provide new insights into the Earth's evolutionary record. This paper also attempts to shed light on the current status of this research and major challenges that lie ahead in the further application of geo-paleo-microbial and organic geochemical research of concretions and their host fossils. Recent efforts to bridge the knowledge and communication gaps in this multidisciplinary research area are also discussed, with particular emphasis on research with significance for interpreting the molecular record in extraordinarily preserved fossils.

Keywords: biomarkers; biominerals; biomolecules; concretion; fossil; microbes; organic geochemistry; paleontology.

Figure 1

The three broad modes of fossilization: ‘Normal’ fossilization, ‘Selective’ fossilization, and ‘Exceptional’ fossilization. Fossils in concretions can be preserved in any of these modes, but those that are exceptionally preserved are of particular interest.

Figure 2

Map of selected geological sites hosting fossiliferous concretions. Particularly prominent sites are summarized in Table 1, although others mentioned in the text are also included here.

Figure 3

Concretions from various sites that host exceptionally preserved fossils. (A) Ichthyosaur [cf. Platypterygius australis (McCoy)] jaw and teeth preserved within a concretion from the upper Albian Toolebuc Formation of Richmond, Queensland, Australia. (B) Several fossils from the Upper Carboniferous Francis Creek Shale Member of the Carbondale Formation of Mazon Creek, Illinois, USA. From left–right: the enigmatic animal Tullimonstrum gregarium Richardson; the fern Pecopteris sp.; the horsetail Annularia steelata; and the fern Diplozites unita. (C) Partially prepared skeleton of the lungfish Griphognathus whitei from the Middle–Upper Devonian Gogo Formation of the Canning Basin, Western Australia (photograph A. M. Clement). (D) Concretions in the field being inspected during fieldwork focused on the Middle–Upper Devonian Gogo Formation, Canning Basin, Western Australia (photograph J. A. Long).

Figure 4

Microbially mediated carbonate concretion formation by different microbial pathways: (A) Ureolytic pathway; (B) Photosynthetic pathway; (C) Sulfate reduction pathway; (D) Methane oxidation pathway; (E) Carbonate precipitation on microbial cell walls; and (F) Carbonate precipitation via microbial EPS (Created with BioRender.com).

Figure 5

Schematic of photic zone euxinia conditions, calcium carbonate concretion formation and in-situ fossilization, demonstrating the complex eogenetic (water column) and diagenetic (sediment/water interface) processes which can be interpreted from molecular biomarkers. (A) An OM nucleus (e.g., a shrimp) in the water column can produce cholesterol by dealkylating sterols (e.g., C₂₉ stigmasterol) from an algal diet. The δ¹³C value of this cholesterol is representative of the average δ¹³C value of the sterols from the dietary sterols in algae. (B) Toxic H₂S might have caused the death of the organism. Bacterially derived EPS build an envelope around the decaying carcass. (C) EPS promote calcium carbonate precipitation around the nucleus, halting further OM degradation early in diagenesis. (D) The carcass becomes fully encapsulated in the calcium carbonate matrix, promoting rapid (days–weeks–months) preservation of soft tissue and biomarkers/biomolecules. (E) Where light reaches the anoxic zone of a stagnant water column and H₂S produced by bacterial sulfate reducers reaches the sunlit zone, PZE conditions develop, where anaerobic phototrophs can flourish. These include Chromatiaceae (purple pigmented sulfur bacteria) and Chlorobiaceae (green-green and green-brown pigmented sulfur bacteria) in a distinct zonation, which synthesize specific carotenoid pigments, including (but not limited to) okenone, chlorobactene, and isorenieratene, respectively. (F) These carotenoids can be incorporated into organosulfur compounds (OSCs) intermolecularly or intramolecularly bound in the soft tissue, or; (G) they can be reduced to stable hydrocarbons. Both of these processes provide specific biomarkers which can indicate the role of PZE and SRB in calcium carbonate formation and fossil preservation. (H) n-alkanes with depleted δ¹³C values (e.g., −40 to-36 ‰) can be indicative of SRB. (I) Chemical reactions of bacterial sulfate reduction forming H₂S, and calcium carbonate precipitation. (J) Diagenetic breakdown of cholesterol into stable steroids via a range of intermediates, illustrating diagenesis as described by Mackenzie et al. (1982). Structures shown represent the full suite of diagenetic breakdown products of cholesterol as identified in a calcium carbonate concretion containing a crustacean by Melendez et al. (2013a). The high percentage abundance of cholesteroid biomarkers was used to identify the fossilized organism as a crustacean. This study was demonstrative of the wealth of information which can be extracted from organisms which can be preserved under favorable conditions, such as within carbonate concretions.

Figure 6

Visual representation of the factors involved in formation of iron carbonate concretions in freshwater influenced environments. Sample used as an example is an iron carbonate concretion from the Mazon Creek Lagerstätte containing an Odontopteris aequalis seed fern. (A) Proposed phases of concretion growth promoted by decay of an OM source: (i) An organic nucleus, such as a leaf, is deposited near the sediment–water interface, and decay results in OM breakdown; (ii) Oxidized OM forms bicarbonate ions, which seep outwards (e.g., Yoshida et al., 2015, 2018), which could then react with Fe²⁺ in surrounding pore-waters. Siderite precipitation forms a ‘proto-concretion’, encapsulating the specimen and the OM; and (iii) Siderite cementation results in formation of a nodule containing a soft tissue fossil. (B) Equations representing the chemical reactions involved in OM oxidation and carbonate formation: (iv) In settings such as freshwater environments, where sulfate is limited, BSR may or may not occur. When it does, it is dependent on sulfate abundances in the pore-water and proceeds only until sulfate is consumed. The reduced sulfate will react with iron and form pyrite via iron monosulfide (e.g., Berner, 1985); (v) Once bacterial sulfate reduction ceases, OM oxidation occurs via iron reduction and methanogenesis; and (vi) This (provided conditions such as pH are suitable) promotes iron carbonate precipitation. Carbonate concretion growth is proposed to proceed until the OM is exhausted (e.g., Baird et al., 1986; Yoshida et al., 2015, 2018).

Figure 7

Flow diagram for analytical methods applicable to microbial fossil concretions, modern and ancient.

Figure 8

Completing the story of fossilization. Conceptual framework to establish fossilization processes and interrogate their biochemical record. The framework combines the complementary analysis of real samples (Approach 1) with those produced under carefully controlled laboratory conditions (Approach 2).