Oolitic Limestone Induced by Photosynthetic Biofilms in the Xuzhuang Formation of Nangao Section, North China

Abstract

The role of biofilms in the formation of ooids is a focal point of current research. This study synthesizes macroscopic data with microscopic observations to analyze the depositional environment and genesis of oolitic limestone within the Xuzhuang Formation at the Nangao section. Notably, cerebroid ooids with unique cortical morphologies have been discovered. Within the nucleus, cortex, and the lumps among the ooids, a high-density preservation of Girvanella has been identified. Clotted micrite structures have also been observed within the filler content. The findings suggest that phototrophic biofilms have facilitated the formation of oolitic limestone in this profile, offering direct evidence for the connection between the festooned cortical morphologies and biofilms. This study further questions the interpretation of clotted micrite structures as sponge remains. These insights significantly enhance our understanding of the causal factors behind ooid formation.

1. Introduction

Ooids are spherical or ellipsoidal coated grains, often composed of a nucleus made of various particle components and a cortex with concentric laminae or radial fibrous layers. As one of the oldest continuous geological records of sedimentary particles, ooids have been widely distributed in geological records since the Archean and have been extensively studied for more than two centuries [1]. The classification, formation process, diagenesis, and evolution of ooids remain a challenging scientific problem. Although increasing evidence suggests that the formation of ooids is a biologically regulated process, some views believe the process of ooid formation to be inorganic [2].

A well-known model is the “Snowball theory”, proposed by Sorby [3], which emphasizes that ooids are formed by the binding of sedimentary particles on the mucilage layer on the surfaces of seafloor debris particles during the rolling process. Another sedimentary model emphasizes the simple physicochemical process of ooid formation. Linck [4] experimentally verified the inorganic origin of ooids, synthesized ooid-like spheroids, and emphasized the typical conditions for ooid deposition in later literature: (1) warm tropical shallow waters; (2) carbonate-saturated seawater with normal or higher salinity; (3) agitated water (e.g., tidal, wave), allowing CO₂ degassing to occur; (4) the presence of various debris particles to provide nuclei for ooids; and (5) a hydrological environment capable of preserving ooids. This sedimentary model considers that the minerals of ooids are directly precipitated from seawater, forming amorphous calcium carbonate (ACC) during the active (jumping, rolling) stage of ooids, continuously colliding and eroding in the turbulent water body to form concentric laminae, and forming radial fibrous calcite around the particles during the quiescent stage [5].

The study of biological roles in the formation process of ooids can be traced back to Wethered [6] discovering Girvanella in ooids, which is one of the most widely known calcified cyanobacteria in the Palaeozoic [7]. Girvanella-group fossils typically occur as individuals or in small clusters, morphologically manifesting as tangled filamentous bodies, and are often found within microbialites. Modern research began at the turn of the century, with a visionary viewpoint proposed by Tucker and Wright [8]: ”Many ooids, usually classified as chemically formed, are either directly biogenically formed or their growth may be biochemically influenced”. Inspired by this viewpoint, a series of new concepts were born: (1) the benthic process in the formation of ooids, which can be summarized as carbonate mineral deposition induced by the degradation of extracellular polymeric substances (EPS) [9] ; (2) radial ooids induced by strong sulfate reduction reactions during organic matter degradation; (3) radial ooids induced by high bacterial activity under nutrient-rich conditions [10]; (4) the hypothesis of ooid formation being nourished by biofilms [11] ; (5) and microbial roles in the formation of ooids [12]. These new concepts attribute the biogenicity of organominerals in ooids to biologically induced mineralization mechanisms and passive mineralization mechanisms of organic matter under biological influence [13]. The biologically induced mineralization mechanism emphasizes that the formation of minerals in ooids is caused by biological metabolic activities or by-products of metabolic activities, which change the alkalinity and ion activity in the environment, thereby inducing the formation of minerals. The passive mineralization mechanism of organic matter under biological influence emphasizes that changes in the external environment, not biological activities, create conditions for mineral precipitation (for example, increased alkalinity), so the participation of living organisms is not required, and EPS provides a template for mineral nucleation during the mineralization process.

The routes of ooid formation can be summarized as benthic and suspension or transport processes [14,15]. The benthic process mainly occurs inside the biofilms, leaving residues of biofilms in the cortex, nucleus, or dense micrite between the ooids. The suspension or transport process occurs in the water body, and the final product consists of ooids and sparry cement that have been transformed, both by construction and by destruction.

Cerebroid ooids, we found, were first discovered by Carozzi [16] in the rocks of the Mississippian Subsystem; they have a festooned shape, and their cortex is composed of wedge-shaped radial fibrous calcite and dark micrite calcite. It is believed that their irregular cortex morphology may be due to the uneven transformation of calcite during the conversion process from aragonite to calcite. Another view is that the cortex of a cerebroid ooid is considered to be influenced by erosional discontinuities produced during the transformation process [17]. Recent studies have suggested that cerebroid ooids are the result of the combined action of biofilm accretion and syngenetic mineral growth. When the effect of syngenetic mineral growth dominates the mineralization process of biogenic deposition, the irregularity of the ooid nucleus will be amplified by mineral growth, forming cerebroid ooids. When biofilm accretion dominates, the internal irregularities will gradually weaken under the influence of surface tension on the biofilm, eventually forming cerebroid ooids [18]. Other evidence includes scanning electron microscope observations of cerebroid ooids, which have found a large number of microbial fossils in the ooid interior and surrounding mud crystal matrix, and that the cortex has an elemental composition similar to that of biofilm calcification products [19].

Ooids are products of a complex process controlled by both biological and physicochemical actions. Cerebroid ooids, due to their distinct characteristics, may represent a unique process of ooid formation. Research has explored the role of biofilms in the formation process of cerebroid ooids through the study of field stratigraphic sequences and depositional environments of samples, as well as full-scan observations under single-polarizing microscopes in the lab.

2. Geological Setting

Phanerozoic sedimentation in the North China Platform directly overlies the underlying Precambrian sedimentation, forming a massive unconformity [20]. It transitions from the mixed succession of red beds and carbonate rocks in Series 2 to the carbonate deposits dominated by oolitic shoals in the Miaolingian (Figure 1a), and ends at the carbonate platform dominated by carbonate mud in the Furongian. The Miaolingian Series in the North China Platform consists of the Maozhuang, Xuzhuang, Zhangxia, and Gushan Formations (Figure 2a) [21].

The Nangao section (Figure 1c) is located in the area from Nangao Village to Beigao Village in Liubu Town, Jinan City, Shandong Province (Figure 1a,b), extending northeast along the road with a stratum dip angle of approximately 5° to 10°. The Cambrian Xuzhuang Formation and Zhangxia Formation extend for about 8 km. The Xuzhuang Formation of the Nangao section is drowned unconformably on the strata of the Maozhuang Formation, forming a third-order sequence (Figure 2a), and is further divided into three system tracts: (1) the lower part is purple and purplish-red silty mud shale and dolomitic mud shale (Figure 2a), with a small amount of calcareous siltstone and sandy dolomite lens and lens layers. This set of strata, similar to red beds, is about 65 m thick, constituting the transgressive system tract (TST) unit of the third-order sequence. (2) The middle part is gray-green and dark gray calcareous mud shale (Figure 2b), about 20 m thick, comprising the condensed section (CS) unit of the third-order sequence. (3) The upper part is thick-layered, blocky oolitic limestone. The lower part is thick-layered blocky oolitic limestone and muddy micritic limestone. Thin layers constitute subtidal-type meter-scale cycles, forming the early highstand system tract (EHST) unit of the third-order sequence. Above, this changes into blocky layers, developing large-scale cross-stratification and frequent scour surfaces in the oolitic limestone, showing high-energy deposition. This constitutes a late highstand system tract (LHST) unit or a forced regression system tract (FRST) unit of the third-order sequence, with a total thickness of about 60 m. This clearly reflects the process of the relative fall in sea level that occurred during the formation of the oolitic shoal. This is consistent with the falling stage system tract model advocated for by Schlager and Warrlichw [23] and corresponds to the higher sediment production action with slower erosion and a base-level drop rate.

3. Materials and Methods

Research samples were collected from some recently abandoned quarries located near the mountain roads of Nangao Village. The Xuzhuang Formation within these quarries is well-developed and features fresh profiles, ensuring that the biogenic fossils within the samples can be clearly identified (Figure 3d). As one of the sources of Cambrian carbonate micrite [23], Girvanella is often preserved alongside micrite in the samples; hence, darker samples were selected. Additionally, as a photoautotrophic microorganism, Girvanella is more likely to be found in shallower depositional environments, so samples with scour surfaces were also collected. The preservation of Girvanella fossils is attributed to the calcification of the Girvanella slime layer, a process interpreted as a response to photosynthesis altering the carbonate equilibrium of precipitation and dissolution in the surrounding microenvironment [24]. The impact on environmental pH levels and the activity of photosynthetic enzymes on Ca²⁺ activity may be key factors. Microphotographs of the samples were taken using a German Zeiss Axio Scope A1 microscope, and whole-slide scanning photographs were captured with a Chinese MTW SD300A microscope.

4. Macroscopic Features

The blocky oolitic limestone (Figure 3d) at the top of the Nangao section (Figure 2b) is characterized by frequently developed scour surfaces (Figure 3a,b), with the ooids on the scour surfaces showing normal grading (Figure 3c). This indicates a strong and turbulent flow environment (due to, e.g., storm flow, tidal flow) [25]. Upon visual inspection, the ooids were observed to be divided into micrite ooids and ooids with sparry edges (Figure 3c), with most ooids being smaller than 2 mm. These features suggest that this set of blocky oolitic limestone, approximately 30 m thick, was formed in a high-energy depositional environment in the subtidal zone. This is similar to the reported formation environment of modern radial ooids [2] but differs from the previously reported cerebroid ooids formed in calm suspension [26]. This expands the environment in which cerebroid ooids appear, and also questions the cerebroid ooid genesis model based on low-energy deposition.

5. Microscopic Features of Cerebroid Ooids

Unlike the upper Xuzhuang Formation, formed by ordinary radial ooids in other areas of the North China Platform, the formation of oolitic limestone dominated by cerebroid ooids in the Nangao Section (Figure 4a) is distinctive. The diameter of the ooids is generally 1~2 mm, gradually becoming normally graded upwards. Cerebroid ooids have bioclastic debris, dark mud crystal nodules, or other small radial ooids as their nuclei (Figure 4a). The cortices generally consist of radial wedge-shaped calcite internally and concentric radial calcite externally [27]. The concentric laminae are dark micrite, and the radial laminae are wedge-shaped calcite (Figure 4c). The ooid cortex is not smooth and presents a petal or cerebroid pattern, distinguishing it from ordinary radial ooids or concentric radial ooids [17]. The section also shows some fully or partially dolomitized ooids (Figure 4d), with dolomite in the ooids displaying a distinct, sugar-like, “foggy nucleus and bright edge” texture, with diameters between 20 and 50 μm. This represents a special shallow burial and evaporation process during the formation of the ooids [28]. Partial dolomitization often occurs at the nuclei of the ooids, representing a kind of heterogeneity in the original composition of the ooids. The thin section also contains completely calcified metamorphosed ooids (Figure 4b). Unlike dolomitized ooids, the grains of calcified metamorphosed ooids are larger, often above 50 μm, indicating a particular diagenetic process.

There are three types of interstitial material between the ooids: (1) fine-grained sparry calcite cement (Figure 4a), showing a comb-like appearance around the ooids, which also provides evidence for the deposition of ooids in a high-energy environment; (2) a matrix composed of dense micrite, which is often considered to be the residue of biofilm calcification; and (3) micrite dominated by vermiform and peloidal structures.

5.1. The Girvanella Filaments in Ooid Nuclei

The dense micrite lumps in the ooid nucleus are highly irregular (Figure 4c and Figure 5a,c), with the largest lumps reaching up to 500 μm. There is a clear boundary between the nucleus and the cortex. The cortex, directly enveloping the ooid nucleus, is generally composed of radial fibrous calcite, with a thickness typically ranging from 100 to 200 μm. Outwardly, there is an alternating occurrence of concentric micrite laminae and radial fibrous calcite laminae, with the cortex as a whole presenting a petal-like or cerebroid appearance (Figure 5a). Under high magnification, the dense micrite in the ooid nucleus appears as densely preserved entwined Girvanella filaments (Figure 5b,d), with filament widths of about 10 μm, composed of dark micrite tube walls and fine, filamentous microtubes. The radial fibrous calcite directly adjacent to the ooid nucleus presents a radial arrangement around the ooid nucleus.

5.2. The Girvanella Filaments in Ooid Cortices

Girvanella filaments are radially arranged within the thicker dense micritic laminae of ooid cortices (Figure 6a), while it is absent in the thinner ones. The filamentous bodies of Girvanella filaments are often truncated (Figure 6b), a phenomenon that may result from erosional processes. The distribution of Girvanella filaments within the ooid cortex is uneven, and the morphology is irregular.

5.3. The Girvanella in the Lump

In the Nanga profile, some lumps or clots composed of dense micrite also appear in the oolitic limestone (Figure 7). Clots are defined as discrete clumps of micrite [29], which are difficult to distinguish from micrite lumps through observation. In the following section, these micrite particles are collectively referred to as lumps. The number of lumps in the profile is not large, and they are generally strip-shaped and larger in size than the nuclei of ooids, with lengths up to 1 mm and widths of 200 μm. Some lumps are encased by radial fibrous calcite, similar to the ooid cortex (Figure 7c). Under high magnification, the lumps show more clearly preserved high-density Girvanella filaments (Figure 7b,d), and the composition of Girvanella filaments in the lumps also includes Subtifloria [7]. Opaque pyrite particles can also be seen in the lumps, representing a possible trace of atypical sulfur bacterial activity.

5.4. Structure Diversity of Cerebroid Ooids

Cerebroid ooids have a variety of nuclei: (1) dark micrite lumps of high-density preserved Girvanella filaments (Figure 4c and Figure 5); (2) bioclasts (Figure 8c (2)); (3) small radial ooids (Figure 8a); and (4) nuclei composed of composite particles (Figure 8d and Figure 9a (1)) and cortex forms. The latter consist of (1) thicker inner rings of radial fibrous calcite that is closely adjacent to the ooid nucleus (Figure 8a), changing the outward appearance of radial concentric laminae to an alternating pattern; (2) radial fibrous calcite cortices appearing to be closely connected to the ooid nucleus (Figure 8c (1), while the cortex itself is not smooth; and (3) concentric radial laminae appearing directly around the nucleus, with no obvious inner or outer ring layers, and thinner formed ooid cortices (Figure 5c and Figure 8b,d).

The key factors determining the morphology of the ooid cortex may be the type, morphology, and size of the ooid nucleus (Figure 4a). (1) Ooids with bioclasts as the nuclei (this type of nucleus can also be explained as a smaller ooid nucleus) or smaller ooid nuclei tend to form ooid cortices with inner and outer ring layers (Figure 8a,c); (2) larger ooid nuclei tend to form cerebroid ooids with direct concentric radial cortices (Figure 5c and Figure 8d); and (3) cerebroid ooids with radial cortices are more like radial cerebroid ooids that have not formed an outer ring layer. The cortices of cerebroid ooids show a dependence on the shape of the ooid nucleus, either retaining the irregularity of the ooid nucleus (Figure 5c and Figure 8a) or amplifying its irregularity (Figure 5a and Figure 8c,d). The irregularity is often amplified by concentric radial layers (Figure 4c).

5.5. Inter-Ooid Filler Content

The dominant type of inter-ooid filler content in the Xuzhuang Formation is ctenoid calcite cement (Figure 4a and Figure 8c,d), but a large amount of the dark micrite matrix (Figure 4a) and clotted micrite (Figure 4a and Figure 9a,b) can also be seen. In some areas, these components can even be the dominant type of filling. Dense micrite and lithified algal structures are distributed in two different areas. The distribution of output in dense micrite is uneven, without bird eye structures, and it is denser compared to lithified algal structures. The type of support in oolitic limestone within dense micrite is grain support. The areas dominated by clotted micrite (Figure 4a and Figure 9a) seem to serve as supports between ooids and do not exhibit the characteristics of inducing the formation of thicker calcite precipitation around ooids or bioclasts, as seen in dense micrite (Figure 8e). These characteristics suggest that the clotted micrite between ooids has different properties from the dense micrite, and also hint at different origins of clotted micrite and dense micrite. The clotted micrite between ooids appears in a layered output, is altered by diagenesis downwards without showing clear boundaries (Figure 4a and Figure 9a), and has a thickness of about 2–3 mm. There are also small plate-like outputs of clotted micrite between the ooids (Figure 4a). The bright tubular forms in the clotted micrite are irregular, with widths between 50 and 100 μm, and they appear nearly parallel to the boundaries of the clotted micrite.

6. Discussion

The frequent appearance of scour surfaces and the overlying normal grading on the surface of oolitic limestone in the Nanga section both indicate that the oolitic limestone was formed in a high-energy environment. During the continuous sea retreat in the late highstand systems tract, frequent sedimentary bottom destruction may have a destructive effect on the in situ-attached benthic microbial mats. Microscopically, this results in lumps, bioclasts, and the release of irregular benthic radial ooids similar to modern ones within the biofilm [30]. These radial ooids are often small (less than 200 μm), forming the nuclei of ooids or existing independently. The lumps produced by the destruction process have Girvanella filaments that are truncated at the edges and irregular in shape. They may preserve some EPS bioactivity, which hinders the nucleation and crystallization processes of calcite [29], avoiding the formation of cement crystalline calcite. Small lumps or those in which the EPS has lost its activity can be covered by new biofilms or produce cement crystallization, forming the nuclei of ooids or lumps wrapped by radial fibrous calcite. The calcified Girvanella filaments in the lumps and ooid nuclei may be the result of calcification occurring on the surface of benthic cyanobacterial cells or within the bacterial slime layer [31]. The slime layer is a structural form of cyanobacterial EPS, providing support for cells, maintaining physical and chemical environmental stability, and preventing predation. This microbial calcification may not depend on carbonic anhydrase (CA)-mediated organomineralization, which relies on the operation of the CO₂ concentrating mechanisms (CCM) [32] and requires lower CO₂/O₂ in the environment [33]. This is inconsistent with the high-CO₂ and low-O₂ atmospheric environment of the Cambrian Furongian [34]. At the same time, the origin and evolution of the CCM in other photosynthetic organisms may come from a series of endosymbiosis and the decoupling of the origin of photorespiration and the CCM, making the timing of the origin of the CCM still controversial [33]. The earliest estimated origin is later than the well-preserved sedimentary record of ooids [35].

The products of early biofilm destruction may also include a large amount of organic micrite that forms dark micrite during degradation, or forms organic films that wrap around other debris. The ctenoid crystallization on bioclasts, lumps, and small ooids can be produced by processes within the microbial mat. This process can be explained as a result of high carbonate supersaturation which is caused by intense photosynthesis and the effective inhibition of precipitation by primitive EPS [13]. This combination of factors leads to the deposition of radial fibrous calcite at only a few locations where the inhibitory effect is overcome and nucleation points exist, i.e., around the nuclei of pre-existing microcrystalline calcite. This radial calcite can also be produced during the suspension or transport processes, as heterotrophic bacterial communities form radially precipitated calcite particles on cell surfaces under conditions of high organic matter enrichment in the environment [36].

The fundamental difference between cerebroid ooids and general radiating concentric ooids lies in the rippled cortices and the non-smooth surfaces [16]. This non-smoothness means that the cortices of cerebroid ooids cannot be interpreted as forming concentric structures due to the wear and redistribution of ooid surface material during the rolling and collision processes, as is the case with general concentric radiating ooids. Cerebroid ooids were thought by early researchers to originate from the uneven conversion of aragonite layers to calcite, and were also generalized as a structure of internal recrystallization. This process obviously cannot explain the formation of Nanga cerebroid ooids in the calcite sea.

Previous studies have summarized a series of the important characteristics of cerebroid ooids: (1) the high-salt, shallow-water environment where cerebroid ooids are produced [26]; (2) the special cortices of cerebroid ooids and their production environment, which are related to the biofilm [19]; and (3) the fact that cerebroid ooids have a variety of production forms [37]. The ooids of Nanga have the following additional characteristics: (1) residual calcified biofilm residues between the nuclei of the ooids and the ooids, and (2) a correlation between the ooid cortex and the nucleus of the ooid. As Coppa et al. [17] stated, the formation of ooids may consist of complex sedimentary processes, and the cerebroid ooids in the Nanga section also undergo complex processes. This complexity is reflected in the diversity of the cortices and nucleus of cerebroid ooids. Some cerebroid ooids with small radiating ooids in the inner cortex and nucleus, and some cerebroid ooids with small biological debris as the nucleus, may radiate ooids induced by in situ biofilms. The formation of the radiating cortex is affected by the inhibition of crystallization by EPS, the promotion of crystallization by EPS during degradation [13], and possibly uneven crystallization caused by the surrounding climate. This process may be similar to the biological debris covered by radiating calcite in Figure 8e.

In the later stage, due to the drop in sea level, the biofilm was repeatedly destroyed by scouring, and these particle components were released, producing small radiating ooids, biofilm debris, biological debris covered by radiating calcite, and some particles captured and adhered by the biofilm. Most of these particles in the water are re-wrapped by biofilm debris that retains some biological activity. And this evidence of re-wrapping is reflected in the residual Girvanella filaments in the festooned cortices. These biofilms produce brain-patterned cortices under the combined influence of syngenetic mineral growth and intra-biofilm sedimentation, as described by Batchelor et al. [18]. The wrapping of the biofilm produces residual Girvanella filaments. Some fragments of the biofilm form lumps between the ooids. These lumps may be too large to be dragged by the water flow, or they may be prevented from nucleating minerals and adhering to other biofilms due to the retention of biological activity.

The clotted micrite structure describes the structure of sparry microtubules in dense micrite [38], often interpreted as Keratosa or Keratolite [39]. The sparry, filamentous bodies are interpreted as (1) calcified residues of keratin fibers in keratin sponges [39]; (2) siliceous sponges [40]; (3) cyanobacteria of the order Nostocales [41]; (4) microbial-mediated clot-like micrite [42]; or (5) a type of metazoan trace fossil [43].

The clotted micrite structure in the Nanga section is different from the most typical clotted micrite structure that is described [41], because (1) the widths of the sparry microtubules in the clotted micrite structure are too thick (generally about 15–50 μm), and (2) the sparry microtubules in the clotted micrite structure rarely bend. But this phenomenon has also been interpreted as an example of the clotted micrite structure [44], or as another form of expression of the same phenomenon described by the clotted micrite structure [45]. The clotted micrite structure in this article is different from the bird eye structure in that the sparry microtubules are not round, and they are also smaller in size. The clotted micrite structure poses difficulties in terms of genetic interpretation [46]. The main evidence for interpreting the clotted micrite structure as a sponge includes the following [47]: (1) under the cooperation of microscopic structure and 3D scanning results, the clotted micrite structure has a similar shape and branching style to the skeleton of keratinous sponges; (2) sponges have a wide cooperative relationship with microbial reefs, and clotted micrite structures are also most often found in stromatolites; (3) degraded sponges can be found in modern microbial reefs; (4) possible biomarker compound evidence has been found that implies an earlier appearance age of common sponges (635 Ma), although this is still later than the earliest appearance time of clotted micrite structures (890 Ma) [48] and similar to the appearance age of the earliest sponge animal body fossils (Guizhou Shibeihai Sponge) (600 Ma) [49].

But this statement also has some difficult-to-explain problems: (1) the clotted micrite structure rarely shows the most typical chimney structure of common sponges; (2) the appearance age of the clotted micrite structure is too early; and (3) there are multiple interpretations of biomarker compounds. The main evidence supporting the siliceous sponge is the discovery of structures that are similar to siliceous sponge spicules, which cannot explain the calcification principle of siliceous spicules. The support for cyanobacteria is the discovery of the phenomenon of clotted micrite structures in various microbial rocks. The main evidence supporting the mud crystal clumps are the huge cavities closely connected to tiny sparry microtubules in the clotted micrite structure, making the clotted micrite structure appear to resemble a small cave, challenging the interpretation of sponges. The problem with this statement is that it is difficult to explain how complex and precise networks are formed by tightly stacked clumps. The interpretation of clotted micrite structures also involves the overgeneralization of the scope of phenomenon interpretation. Different manifestations of clotted micrite structures may have completely different properties, such as: (1) sparry microtubules are uneven in thickness and less likely to bend, and filamentous bodies are generally thicker (generally greater than 50 μm [45], Figure 9); and (2) filamentous bodies are thin and uniform, often bending, and sometimes have strong continuity. The results of 3D scanning are often aimed at the second type of clotted micrite structure [47] and cannot be used to explain the cause of the first type of clotted micrite structure due to obvious differences under the microscope. Moreover, the skeletons of keratinous sponges or siliceous sponges cannot explain the unevenness of the thickness of the sparry microtubules in this clotted micrite structure.

The clotted micrite structure in the Nangao Section is produced in an environment with high detrital input, which is often not suitable for filter-feeding sponges to survive [50]. In addition, the Girvanella filaments in the ooid core and the lumps between the ooids also imply that the clotted micrite structure, which serves as the matrix of brain-patterned ooids, may have the properties of a possible cyanobacteria biofilm. The supporting role of the clotted micrite structure of the Nangao Section oolitic limestone for ooids may suggest that it may be a characteristic of the superficial layer of the biofilm. This biofilm might be similar to the in situ biofilm found by Suarez [30] in the central Pacific atoll, where cerebroid ooids produced within the biofilm were also located. The clotted micrite structure might be a calcified biofilm influenced by organisms, with the following evidence: (1) the cerebroid ooids and other radial ooids produced in dense micrite have been confirmed to be composed of a variety of calcified microbial microfossils and calcified EPS [19]; (2) the irregular shape of the sparry filamentous bodies in the clotted micrite structure of Nangao section makes other interpretations challenging to accept [29]; and (3) the production of calcified biofilms is often similar to the dense micrite of the clotted micrite structure in the Nangao Section [13].

The perspective that supports interpreting clotted micrite as microburrows suggests that it represents traces of primordial parenting skills [43]. The research has identified smooth, egg-shaped bodies within the microburrows, which may signify an ancient nesting behavior. However, this interpretation faces certain challenges, such as the difficulty of determining the species of the nesting organism. Whether the high-energy depositional environment of the Nangao Section was conducive to such nesting activities remains to be further investigated. Nevertheless, this explanation should still be considered as a plausible causal interpretation.

7. Conclusions

The oolitic limestone dominated by cerebroid ooids in the Xuzhuang Formation of the Nangao Section was formed under the conditions of tidal currents during the sea level drop period. Cerebroid ooids form during the repeated destruction process of benthic biofilms were dominated by cyanobacteria.

The type, size, and shape of the cerebroid ooid nucleus are key factors affecting the morphology and form of the cortex. These ooids undergo a benthic process to form a thicker radial fibrous calcite lamina in the nucleus or inner cortex. They are wrapped by biofilms during the suspension process, and external cortices of the cerebroid form are formed under the combined influence of syngenetic mineral growth and internal deposition in the biofilm.

The clotted micrite observed in the Nangao section may consist of calcified microbial residues rather than sponges. The sparry microtubes within the clotted micrite are likely the result of tubular cavities near the surfaces of the microbial films being infilled.