Mesoproterozoic Biogenic Thrombolites from the North China Platform

Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 DOI 10.1007/s00531-012-0817-9

ORIGINAL PAPER

Mesoproterozoic biogenic thrombolites from the North China platform

Dongjie Tang • Xiaoying Shi • Ganqing Jiang

Received: 10 March 2012 / Accepted: 11 August 2012 / Published online: 23 September 2012 Ó Springer-Verlag 2012

Abstract Thrombolites are abundant in the subtidal stages: (1) organomineralization of the cores through dolostones of the Mesoproterozoic Wumishan Formation replacement of organic matter by minute organominerals (ca 1.50–1.45 Ga) in the North China platform. Three resulting from anaerobic degradation of bacteria and EPS major components are identified within the thrombolites: and (2) inorganic precipitation of the outer layers fostered irregular mesoclots, micritic matrix and spar-filled voids. by an increase in carbonate alkalinity in micro-environ- The mesoclot generally comprises a relatively organic-rich ment due to organic matter decomposition. The thrombo- micritic core and a microsparitic outer layer that consists of lites from the Mesoproterozoic Wumishan Formation may fibrous aragonite (pseudocrystals) with less organic matter. have formed through complex interactions between In the core of mesoclots, abundant fossilized organic microbes and environments and represent the earliest remnants, such as putative coccoidal and filamentous known Precambrian biogenic thrombolites. bacteria and mucus- to film-like extracellular polymeric substance (EPS), are closely associated with organomi- Keywords Mesoproterozoic Á Protogenetic thrombolite Á nerals including nanoglobules and submicron-scale poly- Organomineral Á North China platform hedrons. In exceptionally well-preserved mesoclots, their outer layers commonly contain micropores displaying as bacterial molds and filamentous bacteria fossils. The matrix Introduction of mesoclots consists mainly of micropeloids (20–30 lmin diameter) and minor terrigenous detritus. Some mesoclots Thrombolites are a type of microbialites (Aitken 1967; have denticulate edges and their matrix shows growth Shapiro and Awramik 2006) that are formed through laminations that envelope the outlines of mesoclots. These complex interactions of benthic microbial communities features indicate that the mesoclots are primary and they with environments by trapping and binding of sediment were mineralized earlier than the surrounding matrix. The grains, and/or in situ mineral precipitation (Burne and mineralization of mesoclots may have proceeded in two Moore 1987). They are characterized by having mottled and clotted internal fabrics (Aitken 1967) that distinguish them from laminated stromatolites (e.g., Kennard and D. Tang Á X. Shi (&) James 1986). Opinions regarding the origin of thrombo- School of Earth Sciences and Resources, China University lites, however, are divergent. Earlier study suggested that of Geosciences, Beijing 100083, China the mottled/clotted thrombolitic structures may have e-mail: [email protected] resulted from destruction of laminations in stromatolites by X. Shi metazoans or diagenesis (e.g., Hofmann 1973; Walter and State Key Laboratory of Biogeology and Environmental Heys 1985). Thus, abundant occurrence of thrombolites Geology, Beijing 100083, China since the late Neoproterozoic was often ascribed to the onset of metazoans (e.g., Garrett 1970; Walter and Heys G. Jiang Department of Geoscience, University of Nevada, 1985). A number of subsequent studies, however, showed Las Vegas, NV 89154-4010, USA that primary thrombolites are widespread, not resulting 123 402 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 from disturbed or bioturbated stromatolites (e.g., Kennard formation (Dupraz et al. 2004, 2009; Benzerara et al. 2010; and James 1986). Some researchers further argued that Spadafora et al. 2010; Perri et al. 2012). mesoclots in thrombolites might have derived from in situ In this paper, we report thrombolites from the Mesopro- mineralization of discrete microbial colonies, predomi- terozoic Wumishan Formation (ca. 1.50–1.45 Ga) in Yes- nantly coccoidal microbes (e.g., Kennard and James 1986; anpo area, Hebei Province, China, with focus on their Burne and Moore 1987; Kahle 2001). Study of modern internal microfabrics and organominerals. Ultrastructures in microbialites suggested that the clotted textures in mesoclots and other microbial remains of thrombolites were thrombolites may form in environments with high pro- studied by optical microscopy and Field Emission Scanning portion of eukaryotes such as metaphytes and metazoans, Electronic Microscope (FESEM). Our study confirms that and they are not specifically related to coccoidal microbes the Mesoproterozoic thrombolites are of biogenic origin and (Feldmann and McKenzie 1998). It has been also empha- their internal microfabrics are transitional between those sized that taphonomic factors, rather than the presence of found in Phanerozoic and Paleoproterozoic thrombolites eukaryotes, may control the formation of thrombolitic (Kah and Grotzinger 1992), similar to those ‘‘hybrid texture in microbialites (Turner et al. 2000; Planavsky and microbialites’’ proposed by Riding (2008, 2010). Ginsburg 2009). Other researchers further pointed out that different microbial communities with particular metabo- lisms may be responsible for the clotted fabrics in modern Geological setting microbial mats (Myshrall et al. 2010; Mobberley et al. 2012). For late Neoproterozoic thrombolites, variable Stratigraphic succession and age constraints microbial groups and environmental conditions have been suggested as the major controls for the clotted fabrics The Mesoproterozoic succession in the North China plat- (Harwood and Sumner 2011). form was deposited in rift and post-rift basins associated with Despite their debatable origin, modern thrombolites the tectonic evolution from the break-up of Columbia to the certainly represent a kind of microbial mat ecosystems assembly of Rodinia. The stratigraphic succession comprises (Myshrall et al. 2010; Jahnert and Collins 2012). Their two large tectono-sedimentary cycles (Fig. 1). The lower ancient analogs, however, have been seldom confirmed to cycle (Jixian Group) is dominated by carbonates, and the be biogenic origin (e.g., Monty 1976; Thompson et al. upper cycle (Qingbaikou Group) is composed of siliciclas- 1990; Soudry and Weissbrod 1995), especially for those tics and black shales. Both the Jixian and Qingbaikou Groups older than late Neoproterozoic (Harwood and Sumner are bounded by regional unconformities. A number of zircon 2011). The oldest thrombolites were reported from the U–Pb SHRIMP ages (Lu and Li 1991; Li et al. 1995, 2010; Paleoproterozoic (ca. 1.92 Ga) strata in NW Canada (Kah Gao et al. 2007, 2008a, b; Lu et al. 2008; Su et al. 2010) from and Grotzinger 1992), but they were interpreted as inor- the succession provide reasonable geochronologic con- ganic sea-floor carbonate precipitates under carbonate straints for the stratigraphic units (Fig. 1). According to the supersaturated and anoxic ocean chemistry (Kah and available age data, the top and base of the Gaoyuzhuang Grotzinger 1992). So far, no thrombolite has been reported Formation are at ca. 1.53 and ca. 1.60 Ga, respectively, and from Mesoproterozoic successions (Grotzinger and James those for the Xiamaling Formation are at ca. 1.30 and ca. 2000; Harwood and Sumner 2011). Therefore, the study of 1.40 Ga (Qiao et al. 2007; Gao et al. 2009, 2010). So far, no Mesoproterozoic thrombolites and their genesis would direct age has been obtained from the Wumishan Formation. provide insights for understanding the interactions between However, stratigraphic relationship and radiometric ages microbial communities and environments in early Earth from underlying and overlying strata roughly constrain history and the relationship between the secular evolution the Wumishan Formation as early Mesoproterozoic (the of ocean chemistry and change in microbial ecosystems. Calymmian Period) between ca. 1.50 and ca. 1.45 Ga (Gao Revealing the genesis and organomineralization mech- et al. 2009). The Changlongshan Formation is likely younger anisms of ancient thrombolites is challenging, because than 1.0 Ga in age (Gao et al. 2009, 2010) and is early mesoclots, the key feature and framework of thrombolites, Neoproterozoic. Therefore, the upper Mesoproterozoic is have been largely preserved as sparitic or micritic car- very likely absent in most parts of the North China platform: bonate with rare recognizable fossils. It is often difficult to the unconformity between the Changlongshan and Xiamal- identify fossilized bacterial remnants and their related ing Formations represents probably a stratigraphic gap organominerals at the microscopic resolution (Soudry and lasting for *300 Ma. Weissbrod 1995). Recent studies indicate that microfabrics The Wumishan Formation is one of the most widespread and organominerals at submicron and nanometer scales Mesoproterozoic lithostratigraphic units in the North China are critical for understanding the microbial activities and platform. Lithologically, it is largely composed of dolo- their interactions with environments during microbialite stone, with abundant siliceous bands and a variety of 123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 403

Erathem Formation thins to *1,800 m and unconformably contacts Formation Lithology Age (Ma) and references /System with the underlying sandy dolostone of the upper Fujunshan <520 Ma Jingeryu upper cycle Gaoyuzhuang Formation and the overlying black shale of Changlongshan <1000 Ma? the lower Hongshuizhuang Formation. The Yangzhuang Xiamaling Paleozoic Tieling 1372±18 (Su et al. 2010) Formation between the Gaoyuzhuang and Wumishan For- Qingbaikou 1380±36 Hongshuizhuang (Su et al. 2010) 1379±12 mations, which is present in the Jixian area, is absent in the 1366±9 (Gao et al. 2008a) study area.

4 1368±12 (Gao et al. 2007) The ﬁrst member of the Wumishan Formation is mainly

Member 1437±21 (Su et al. 2010)

Neoproterozoic composed of peloidal dolostones with thrombolites and 1400 Ma (?)

3 chert bands that were mostly deposited from intertidal to

Member supratidal environments. The second member is dominated 1000 by thrombolitic and thick beds of laminated dolostones

2 deposited in upper subtidal to intertidal environments. The Wumishan 500

Member c third member is characterized by thick bedded to massive r cycle r thrombolitic and laminated dolostones, with meter-scale 0m

1 lowe parasequences composed of lower subtidal to lower inter-

Jixian Member tidal facies. The fourth member is generally composed of medium bedded, laminated and micritic dolostones. In this

Mesoproterozoi Yangzhuang member, strata show a general thinning-upward trend and

1559±12 thrombolites are gradually substituted by stromatolites in 1560±5 (Li et al. 2010) the upper part, recording shallowing-upward deposition in a prograding carbonate platform (Shi et al. 2008; Tang Gaoyuzhuang et al. 2011).

1600 Ma (?) Sedimentary facies and thrombolite horizons Dahongyu 1625±6 (Lu and Li 1991) 1622±23 (Lu et al. 2008) Sedimentary facies and sequence stratigraphic study indi- c Tuanshanzi 1626±9 (Gao et al. 2008b) 1683±67 (Li et al. 1995) cate that the carbonates of the Wumishan Formation are highly rhythmic and composed of hundreds of meter-scale Chuanlinggou shallowing-upward parasequences. Most of the parase-

Changcheng quences consist of 2–3 identical sedimentary facies (Unit

Paleoproterozoi A–C) (Tang et al. 2011). Unit A is characterized by Changzhougou thrombolitic dolostones (largely tabular thrombolites) that were deposited from subtidal environments. Unit B con- 1800 Ma (?) Qianxi Sanggan sists of laminated dolostones (largely stratiform stromato- limestone marly dolomite limy lites) formed mainly in upper subtidal to intertidal dolomite dolomite environments. Unit C is composed of dolomicrite or marly dolomitic silty mud- shale silty limestone dolomite stone shale dolomicrite deposited mainly from supratidal environments conglomerate volcanic gneiss sandstone /gravel layer granulite (Tang et al. 2011). Parasequences stack into disconformity- bounded sequences of tens to hundreds of meters thick. The asphaltene stromatolite chert chert nodules bands thickness of sequences, parasequences, and their compo- Fig. 1 Stratigraphic subdivisions and zircon U–Pb age constraints of nent facies vary across the North China platform, but their the Proterozoic succession in the North China platform. The SHRIMP vertical stacking patterns are regionally correlatable. ages aside the column are adopted from the references quoted in The general features of a parasequence are shown in parentheses Fig. 3a. Thrombolites mainly occur in the lower unit (Unit A) of the parasequences and most of them are shown as microbialites (Wang et al. 2000; Mei et al. 2001; Zhou tabular forms. Mesoclots in the thrombolites are dark in et al. 2006; Shi et al. 2008; Tang et al. 2011). In general, color but highly variable in both shape and size, most the Wumishan Formation is predominated by peritidal commonly as irregular blocks (Fig. 3b, c) or curved rib- carbonate facies. Its thickness varies considerably. In the bons (Fig. 3d). They intertwine with each other and form Jixian area around Tianjin, the formation is 3,340 m thick upward-growing dendritic structures (Fig. 3e). Thrombo- and can be subdivided into four members. In the study lites with dendritic mesoclots require relatively high area (Yesanpo, Hebei Province) (Fig. 2), the Wumishan accommodation space for their accretion (Kershaw et al. 123 404 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413

Fig. 2 Simpliﬁed geological map of the study area. a Locality of the study area. b Simpliﬁed geologic map of the study area (after Tang et al. 2011)

2011), and they were most likely formed in middle to lower Axio Scope A1 microscope. The ultrastructures were subtidal zone (Jahnert and Collins 2012). Matrix inﬁlled studied using a Zeiss SUPPA 55 ﬁeld emission scanning between mesoclots is dominated by dolomicritic cement electron microscope (FESEM) under 10 kV accelerating but contains minor intraclastic debris (Fig. 3c), indicat- voltage and with a working distance of 3–9 mm. In-lens ing overall low-energy environments with occasional secondary electron imaging detector was used to charac- high-energy events (e.g., storm events). In Unit C of the terize the surface features. To obtain high-quality imaging, parasequences, purple oxidation surfaces, mat cracks both thin sections and freshly broken fragments were used with curled margins (Fig. 3f) and halite pseudomorphs for FESEM observations. Nonconductive samples were (Tang et al. 2011) are common, indicating upper inter- coated with platinum before the analysis. tidal to supratidal environments. Thus, the thrombolite- bearing parasequences (e.g., Fig. 3a) in the Wumishan Formation were deposited from lower subtidal to supra- Macro- and microscopic features tidal environments, recording transgression–regression cycles. Macrostructures

Thrombolites in the study area are domal or tabular in Materials and study methods morphology. Domal thrombolites are composed of clustered mesoclots that form branching patterns with upward Samples studied in this paper are mainly from the middle growth features (Fig. 3e). The domes are commonly part of the Wumishan Formation in the vicinity of Yes- 10–40 cm in width and 10–30 cm in height, but occa- anpo, Hebei Province. Some of the samples have been sionally they form buildups of 3 m high and 6 m wide. The variably silicified during early diagenesis, but they have tabular thrombolites are the most common type in the study well-preserved primary fabrics. In contrast, most of the area and are characterized by diffused mesoclots (Fig. 3b– unsilicified carbonate samples have been recrystallized and d). Despite morphologic variations, domal and tabular their microfabrics are hardly recognizable. thrombolites have three similar internal components Macroscopic features of the thrombolites were studied (Fig. 3b–e): (1) variably shaped gray to black mesoclots— by observations in field outcrops and on polished slabs. their clusters and aggregates constituting the frame- Microfabrics were observed on thin sections with a Zeiss work of thrombolites; (2) gray dolomicritic matrix,

123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 405

Fig. 3 Stratigraphic succession, parasequence and thrombolite fea- with blocky mesoclots. c Thrombolite with blocky mesoclots and a tures from the Wumishan Formation. a Typical architecture of a few intraclasts (arrows) in micritic matrix. d Thrombolite with parasequence. The parasequence comprises three depositional units: ribbon-like mesoclots. e Thrombolite with dendritic mesoclots. thick to massive bedded thrombolitic dolomite (A), medium bedded, f Subaerial erosion surface with microbial mat cracks with curled laminated dolomite rich in silicified microbial mats and small domal margins (arrows) in the uppermost unit of the parasequence stromatolites (B), and thin bedded dolomicrite (C). b Thrombolite commonly surrounding mesoclots or in their vicinity; and (3) Microfabrics spar-filled voids, irregularly scattered in thrombolites. Mes- oclots in the thrombolites have three morphological types: Microscopically, each of the mesoclots comprises a variable blocks (Fig. 3b, c), curved filaments or ribbons micritic core and an outer layer composed of microsparitic (Fig. 3d) and irregular branching columns (Fig. 3e). As fibrous crystals (Fig. 4a, b). The core is usually 200–1,000 shown in Fig. 3d, e, the morphology of thrombolites is related lm in diameter, made up of micrite and micropeloids that to the type and spatial arrangement of their internal mesoclots. are 10–60 lm in diameter and rich in organic matter 123 406 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413

123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 407 b Fig. 4 Internal fabrics of thrombolites. a Three major components matrix (Fig. 5b, c). This feature suggests that the denticu- generally recognizable within thrombolite: irregularly shaped meso- late edge of mesoclots may have formed by storm erosion/ clot (Cl), dark micritic matrix (Mm) and spar-filled void. b Mesoclot generally comprises a relatively organic-rich micritic core (Mc) and abrasion rather than stylolization during diagenesis. For an organic-poor outer layer composed of fibrous aragonite pseudo- some isolated mesoclots within matrix, laminae are seen to crystals (Fa). c A micropeloid in the core of a mesoclot. Nucleus in bend and envelope the mesoclots, but their overlying the micropeloid (in circle) is rich in bacterial relics, whereas its laminae remain straight (Fig. 5e). This implies that the bent encasing rim has little organic matter. d A silicified mesoclot. The core is relatively rich in organic relics and irregular in shape. laminae were not caused by differential compaction, but e Feathery termination of fibrous crystals (arrows) in the outer layer from infilling around earlier lithified mesoclots. Thus, we of a mesoclot. f Possible filamentous bacteria in the outer layer of a believe that the mesoclots are of primary origin, and they mesoclot. g Close view of boxed part in Fig. 4f, showing possible were not resulted from diagenetic lamina destruction of filamentous bacteria (arrow). h Fluorescence photomicrograph of mesoclots, showing orange–red autofluorescence stimulated by stromatolites. organic relics in the outer layers and cores of mesoclots. i Close view of boxed part in Fig. 4a, showing a clear micropeloid in micritic Ultrastructure matrix. The nucleus has dense bacterial relics, while the encasing rim has rare organic matter In silicified thrombolite samples, FESEM observation reveals abundant microspheres, filaments and mucus-like (Fig. 4a–c). Some silicified samples contain amorphous films (Fig. 6a–e) from the core of mesoclots. The micro- and mucus-like films in the cores (Fig. 4d), which are spheres are 0.6–2.4 lm in size and filaments are 1–2 lmin interpreted as fossilized EPS on the basis of their ultra- diameter and up to 10 lm in length. They are found in structures observed under FESEM. The microsparitic layers close association (Fig. 6a) and are possibly coccoidal and surrounding cores are variable in thickness, commonly filamentous bacteria fossils, respectively. The microspheres 1–1.5 times of the diameter of the cores. Although in most and filaments are commonly coated with purported EPS cases, the outer layers have been variably recrystallized, relics (Fig. 6b, e) that contain abundant nanoglobules of some well-preserved examples have primary fabrics con- 20–80 nm in diameter (Fig. 6b–e). These features, how- sisting of fan-shaped aggregates of fibrous microspars that ever, are rarely preserved in the outer layers surrounding are 200–1,500 lm long and radially arranged as isopac- the mesoclot cores. In the outer layers, random micropores hous bands. These microsparitic fibers commonly have are observed (Fig. 6f) and they are inferred as coccoidal irregular extinction and feathery terminations (Fig. 4e). The bacteria molds. These layers are composed of crystals with outer layers also contain minor organic relics. Particularly, perfect cleavage, which are distinctive from the micritic in some well-preserved samples, putative bacterial filament cores. Filaments and other organic relics have been rarely fossils (Fig. 4f, g) can be identified. Under ultraviolet light, identified (Fig. 4f–h), suggesting that the outer layers the outer layers show orange–red autofluorescence likely have an origin different from that of the cores in (Fig. 4h), indicating the presence of organic matter. The mesoclots. matrix between mesoclots is mainly composed of micrope- Micrite in the core of mesoclots is mainly composed of loids of 20–30 lm in diameter. Nuclei in these micrope- anhedral polyhedrons formed by aggregates of nanoglo- loids, though vaguely defined, are largely micrite and rich in bules of 20–80 nm in diameter (Fig. 7a). The nanoglobules putative bacterial relics, whereas the encasing rims are are closely associated with purported EPS remnants and mainly microspar and lack organic matter (Fig. 4i). The coalesce into sub-hexagonal polyhedrons about 200 nm in voids are randomly scattered in thrombolites and are com- diameter (Fig. 7b). The polyhedrons further fuse into monly filled with sparitic dolomite (Fig. 4a). submicron-scale aggregates (Fig. 7c) or micron-scale Parts of the matrix in thrombolites contain distinctive micritic particles (Figs. 6a, 7b). Nanoglobules, polyhedrons laminations (Fig. 5). The laminations are expressed by and micritic particles occur in places where organic relics alternations of thin, organic-rich dark laminae and rela- are present and they commonly replace organic matter tively thicker light laminae that are rich in micropeloids (Figs. 6a, b, d, 7c, d), suggesting that they were derived and microsparitic particles. Such laminar structures are from degradation of organic matter. consistent with mineralized microbial mats. The contacts between the laminae and mesoclots are distinctive, and the laminae are seen to bend around mesoclots (Fig. 5a, b). Discussion This indicates that the mesoclots were mineralized earlier than the matrix. Some mesoclots show denticulate edges Genesis of the Wumishan thrombolites with broken fractures, consistent with their earlier lithifi- cation. The broken fractures are restricted to individual Thrombolites gradually became abundant since the late mesoclots, and they do not penetrate into the surrounding Neoproterozoic. In modern and many Paleozoic examples, 123 408 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413

Fig. 5 Characteristics of matrix in thrombolite. a Matrix (Mm) with mesoclots. Some laminations are microstylolites that track the faint laminations that bend along the mesoclot (Cl) outline. b Lam- microbial laminae. e Close view of the boxed area in Fig. 5a. inations in matrix (Mm) bend along the outline of mesoclot (Cl) that Laminae bend at sides of a mesoclot (dash lines), but the laminae has jagged edges. c Close view of boxed area in Fig. 5b, showing above the mesoclot (arrows) are straight jagged edges (arrows). d Clear laminations in matrix (Mm) between they are considered as a distinct type of microbialites (e.g., stromatolites (e.g., Hofmann 1973; Walter and Heys 1985). Kennard and James 1986; Myshrall et al. 2010). However, In the study area, both thrombolites and stromatolites are thrombolites older than Neoproterozoic are rare and evi- common in the peritidal dolostones of the Wumishan dence for their biogenic origin has been lacking (e.g., Formation. However, they are rarely present together. Grotzinger and James 2000; Harwood and Sumner 2011). Thrombolites mostly occur in the lower units (Unit A) of The macro- and microfabrics from the thrombolites of the parasequences, while stromatolites are mostly present in Wumishan Formation clearly demonstrate a biogenic ori- the middle units (Unit B). Only occasionally they coexist at gin for the Mesoproterozoic thrombolites. the Unit A–Unit B transition (Tang et al. 2011). In some Early studies suggested that thrombolites might be of large reef-like buildups (3 m high and 7 m wide), they secondary origin, formed by lamina destruction of grade into each another vertically or laterally. This

123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 409

Fig. 6 Possible fossilized bacteria and microbially induced structures showing bacterial filament (FB) with grainy surface. d Close view of in mesoclots. a Possible coccoidal (CB), filamentous bacteria (FB) the boxed area in Fig. 6c, showing filamentous bacteria (right) and and micritic particle (MP). b Close view of the small box in Fig. 6a, EPS relics (left) partially replaced by nanoglobules (Ns). e Putative showing possible coccoidal bacteria (CB) *2.4 lm in diameter, filamentous bacteria (FB) and nanoglobules (Ns) associated with EPS. which is covered by nanoglobules (Ns) and entombed in mineralized f Fibrous aragonite pseudocrystals (Fa) with micropores (Mo) mucus-like EPS relics. c Close view of the larger box in Fig. 6a, indicative of potential bacterial molds phenomenon suggests that local environmental conditions diagenetic destruction of stromatolite laminae. Instead, controlled the distribution patterns of thrombolites and shifts from thrombolites to stromatolites most likely stromatolites. The mesoclots in thrombolites show a variety record microenvironmental changes. Since no metazoan of shapes, clear primary microfabrics (Fig. 5) and sharp is known in the Mesoproterozoic, the possibility of contact with their surrounding matrix (Fig. 4a, b, d). These mesoclots originated from metazoan disruption can be features imply that the mesoclots are not resulted from excluded.

123 410 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413

Fig. 7 Organominerals in the core of a mesoclot. a Numerous (Ns). c Clustered polyhedrons (Po) closely associated with mucus-like nanoglobules (Ns) dispersed on purported EPS; some of them have EPS. d Nanoglobules (Ns) closely associated with bacterial ﬁlament clear rims (arrows). b A micritic particle (Mp) formed by sub- and mucus-like EPS relics hexagonal polyhedrons (Po) that consist of coalesced nanoglobules

Mineralization process and formation of mesoclots micritic particles (Figs. 6a, 7b, c) and form micropeloids (Fig. 4c). Aggregation of these micropeloids and micritic Previous study of ancient thrombolites largely focused on particles (Fig. 6a) with interweaving organic remnants their morphology and microscopic textures that provide constitutes a mineralized core (Fig. 4b). It is important to limited information on mineralization and formation pro- note that nanoglobules are closely associated with and cesses (Soudry and Weissbrod 1995). Some studies with partially replaced putative EPS and bacterial remains SEM observations have greatly improved our knowledge (Figs. 6, 7). This relationship imply that the nanoglobules about the ultrastructures in thrombolites (e.g., Thompson were derived from anoxic degradation of organic matter et al. 1990; Soudry and Weissbrod 1995). However, the including both EPS and bacterial biomass (Perri and mineralization process and formation mechanism of the Spadafora 2011; Perri et al. 2012), and they were the mesoclots in thrombolites remain to be clariﬁed. products of organic macromolecules mixed with mineral Mineralization of the core of mesoclots can be inferred precipitates (Young and Martel 2010). The replacement of from their multi-scale microfabrics and ultraﬁne organo- organic matter by nanoglobules and subsequently coa- mineral components (e.g., Spadafora et al. 2010; Perri and lesced polyhedrons are the most important processes in Spadafora 2011; Perri et al. 2012). Our study shows that organomineralization (Sprachta et al. 2001). Similar the core of mesoclots consists mainly of micrites and nanoglobules and polyhedrons have been widely observed micropeloids (Fig. 4b, c). FESEM observation indicates in ancient (Sprachta et al. 2001; Perri and Tucker 2007; that the micrites are mainly composed of submicron-scale Perri and Spadafora 2011; Ezaki et al. 2012) and modern polyhedral crystals or their aggregates (Fig. 7b, c). Poly- microbialites (Dupraz et al. 2004; Benzerara et al. 2006, hedrons are seen to have formed by coalesced nanoglo- 2010; Niederberger and Co¨lfen 2006; Spadafora et al. bules (Fig. 7b, c) and they can further aggregate into larger 2010; Perri et al. 2012), as well as in microbially induced

123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 411 precipitates of culture experiments (Vasconcelos et al. composed of fibrous fabrics shown as isopachous layers. 1995; Warthmann et al. 2000; Aloisi et al. 2006; Bontog- Though fibrous aragonites are abundant in thrombolites, nali et al. 2008). These particles were generally regarded as they virtually do not occur in places where no detectable organominerals that can be used as biosignatures recording organic matter exists. Such an association may imply that interactions between microbial activities and environments the formation of fibrous aragonite in outer layers was also (Dupraz et al. 2004, 2009; Perri et al. 2012). The close related to organic matter, likely templated by bacteria and association of organominerals and organic relics in the EPS (Fig. 4f–h) and stimulated by increased alkalinity in mesoclots of thrombolites indicates the fundamental role of microenvironments through organic matter degradation. EPS and filamentous bacteria played in the mineralization Specifically, they were formed through microbially influ- of the core of mesoclots. enced precipitation (Dupraz et al. 2009). Therefore, the The outer layers in mesoclots are characterized by fibrous aragonitic (pseudocrystals) outer layers of mesoc- fibrous crystals. The fibers have irregular extinction and lots in thrombolites are different from the abiotic sea-floor feathery terminations (Fig. 4e) characteristic of an arago- crystal fans widely recognized from Late Archean to nite precursor (e.g., Sandberg 1985; Peryt et al. 1990; Paleoproterozoic successions (e.g., Kah and Grotzinger Sumner and Grotzinger 2000). Similar fibrous aragonite 1992; Sami and James 1994; Sumner and Grotzinger 1996, crystal fans or crusts were often interpreted as inorganic 2000, 2004; Grotzinger and James 2000). seafloor carbonate precipitates (e.g., Grotzinger and James 2000) or carbonate cements (Kah and Grotzinger 1992; Grotzinger and Knoll 1995). Their abundance in early Conclusion

Precambrian (Ar3–Pt1) carbonate successions was considered to record unusual ocean chemistry in early Earth Thrombolites are abundant in the subtidal dolostones of the history, including 5–10 times higher (than today) dissolved Mesoproterozoic Wumishan Formation (ca 1.50–1.45 Ga), inorganic carbon (DIC) reservoir (Bartley and Kah 2004), North China. Morphologically, they have domal and tab- high concentration of inhibitors (e.g., Fe2?,Mg2?) for ular forms but internally they share similar textures with carbonate nucleation (Sumner and Grotzinger 1996; variably shaped mesoclots, micritic matrixes and spar-ﬁlled

Grotzinger and James 2000) and high CaCO3 supersatu- voids. Mesoclots are composed of organic-rich micritic rated ocean seawater (Grotzinger and Knoll 1995; Sumner cores and organic-poor fibrous outer layers (aragonite and Grotzinger 1996, 2000, 2004; Pruss et al. 2008). In pseudocrystals). The micritic matrix surrounding mesoclots some well-preserved samples of the Wumishan thrombo- consists mainly of micropeloids of 20–30 lm in diameter, lites, microbial fossils exist in the outer layers, including with minor terrigenous detritus. putative filamentous bacteria (Fig. 4f–h) and micropores The mesoclot cores are rich in bacterial filaments, that are reminiscent of coccoidal bacterial molds (Fig. 6f). mineralized EPS, and closely associated nanoglobules and The presence of organic relics (Fig. 4h) in the outer layers submicron polyhedrons. The fibrous outer layer is largely suggests that the aragonite crystal fan-like outer layers may made up of aragonite pseudocrystals with clear cleavage, have been also related to microbial activities, although the with only rarely preserved organic relics and micropores formation mechanism of different carbonate mineral mor- reminiscent of coccoidal bacteria molds. phology between the cores and outer layers requires further The nanoglobules and polyhedrons recognized in the exploration. mesoclot cores are similar to the organominerals found in The close association of organominerals with EPS modern microbialites and in microbial carbonates precipi- (Fig. 7) and bacterial filaments (Fig. 6) in the mesoclot tated in culture experiments. Nanoglobules and polyhe- cores provides evidence for carbonate precipitation con- drons are closely associated with EPS and bacterial current with bacterial decomposition when the thrombolitic filaments. Thus, the core of mesoclots in thrombolites may microbial mats were still alive or freshly buried. The have resulted from mineralization of EPS and bacterial mineralization of mesoclot cores was likely induced by biomass. The outer layers in mesoclots may have derived increased alkalinity resulting from degradation of organic from microbially influenced precipitation. The thrombo- matter via bacteria sulfate reduction (BSR) or other het- lites from the Mesoproterozoic Wumishan Formation are erotrophic processes. Putative bacteria (Fig. 6d) and EPS among the earliest primary biogenic thrombolites reported (Fig. 7d) apparently provided templates and preferable so far. sites for initial carbonate nucleation and precipitation. The organomineralization of the cores seemed to have pro- Acknowledgments The study was supported by the Ministry of ceeded largely through the replacement of organic matter Science and Technology (No. 2011CB808806) and the National Natural Science Foundation of China (No. 40972022 and No. by minute organominerals and their subsequent aggrega- 40921062). We are grateful to Prof. Wolf-Christian Dullo, Editor tion. Most of the mesoclots are enveloped by outer layers in Chief, and two anonymous reviewers for their constructive 123 412 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 suggestions and critical comments that greatly improved the paper. Gao LZ, Ding XZ, Gao Q, Zhang CH (2010) New Geological time Thanks are also given to Drs. Yunpeng Pei, Lin Wang and Wenhao scale of Late Precambrian in China and geochronology. Geol Zhang for their assistance in field work and to Mr. Luo Jun for his China 37:1014–1020 (In Chinese with English abstract) help in the experiment. Garrett P (1970) Phanerozoic stromatolite: noncompetitive ecologic restriction by grazing and burrowing animals. Science 169:171– 173 Grotzinger JP, James NP (2000) Precambrian carbonates: evolution of References understanding. In: Grotzinger JP, James NP (eds) Carbonate sedimentation and diagenesis in the evolving Precambrian world, Aitken JD (1967) Classification and environmental significance of vol 67. SEPM, Special Publication, Tulsa, Oklahoma, pp 3–20 cryptalgal limestones and dolomites, with illustrations from the Grotzinger JP, Knoll AH (1995) Anomalous carbonate precipitates: is Cambrian and Ordovician of southwestern Alberta. J Sediment the Precambrian the key to the Permian? Palaios 10:578–596 Res 37:1163–1178 Harwood CL, Sumner DY (2011) Microbialites of the Neoproterozoic Aloisi G, Gloter A, Wallmann K, Guyot F, Zuddas P (2006) Beck Spring Dolomite, Southern California. Sedimentology Nucleation of calcium carbonate on bacterial nanoglobules. 58:1648–1673 Geology 34:1017–1020 Hofmann HJ (1973) Stromatolite characteristics and utility. Earth Sci Bartley JK, Kah LC (2004) Marine carbon reservoir, Corg-Ccarb Rev 9:339–373 coupling, and the evolution of the Proterozoic carbon cycle. Jahnert RJ, Collins LB (2012) Characteristics, distribution and Geology 32:129–132 morphogenesis of subtidal microbial systems in Shark Bay, Benzerara K, Menguy N, Lopez-Garcia P, Yoon TH, Kaz¢mierczak J, Australia. Marine Geol 303–306:115–136 Tyliszczak T, Guyot F, Brown GE Jr (2006) Nanoscale detection Kah LC, Grotzinger JP (1992) Early Proterozoic (1.9 Ga) thrombo- of organic signatures in carbonate microbialites. Proc Natl Acad lites of the Rocknest Formation, Northwest Territories. Palaios Sci USA 103:9440–9445 7:305–315 Benzerara K, Meibom A, Gautier Q, Kazmierczak J, Stolarski J, Kahle CF (2001) Biosedimentology of a Silurian thrombolite reef Menguy N, Brown GE Jr (2010) Nanotextures of aragonite in with meter-scale growth framework cavities. J Sediment Res stromatolites from the quasi-marine Satonda crater lake, Indo- 71:410–422 nesia. In: Pedley HM, Rogerson M (eds) Tufas and speleothems: Kennard JM, James NP (1986) Thrombolites and stromatolites: two unravelling the microbial and physical controls, vol 336. distinct types of microbial structures. Palaios 1:492–503 Geological Society, Special Publications, London, pp 211–224 Kershaw S, Crasquin S, Forel MB, Randon C, Collin PY, Kosun E, Bontognali TRR, Vasconcelos C, Warthmann RJ, Dupraz C, Richoz S, Baud A (2011) Earliest Triassic microbialites in Curuk Bernasconi SM, McKenzie JA (2008) Microbes produce nano- Dag, southern Turkey: composition, sequences and controls on bacteria-like structures, avoiding cell entombment. Geology formation. Sedimentology 58:739–755 36:663–666 Li HK, Li HM, Lu SN (1995) Grain zircon U-Pb age for volcanic Burne RV, Moore LS (1987) Microbialites: organosedimentary rocks from Tuanshanzi Formation of Changcheng System and deposits of benthic microbial communities. Palaios 2:241–254 their geological implication. Geochimica 24:43–48 (In Chinese Dupraz C, Visscher PT, Baumgartner LK, Reid RP (2004) Microbe- with English abstract) mineral interactions: early carbonate precipitation in a hypersa- Li HK, Zhu SX, Xiang ZQ, Su WB, Lu SN, Zhou HY, Geng JZ, Li S, line lake (Eleuthera Island, Bahamas). Sedimentology 51: Yang FJ (2010) Zircon U-Pb dating on tuff bed from 745–765 Gaoyuzhuang formation in Yanqing, Beijing: further constraints Dupraz C, Reid RP, Braissant O, Decho AW, Norman RS, Visscher on the new subdivision of the Mesoproterozoic stratigraphy in PT (2009) Processes of carbonate precipitation in modern the northern North China Craton. Acta Petrologica Sinica microbial mats. Earth Sci Rev 96:141–162 26:2131–2140 (In Chinese with English abstract) Ezaki Y, Liu JB, Adachi N (2012) Lower Triassic stromatolites in Lu SN, Li HM (1991) A precise U-Pb single zircon age determination Luodian County, Guizhou Province, South China: evidence for for the volcanics of Dahongyu Formation, Changcheng system in the protracted devastation of the marine environments. Geobi- Jixian. Acta Geosicientia Sinica 22:137–145 (In Chinese with ology 10:48–59. doi:10.1111/j.1472-4669.2011.00309.x English abstract) Feldmann M, McKenzie JA (1998) Stromatolite–thrombolite associ- Lu SN, Zhao GC, Wang HC, Hao GJ (2008) Precambrian metamor- ations in a modern environment, Lee Stocking Island, Bahamas. phic basement and sedimentary cover of the North China Craton: Palaios 13:201–212 a review. Precamb Res 160:77–93 Gao LZ, Zhang CH, Shi XY, Zhou HR, Wang ZQ (2007) Zircon Mei MX, Ma YS, Guo QY (2001) Basic litho-faces-succession model SHRIMP U-Pb dating of the tuff bed in the Xiamaling Formation for Wumishan cyclothems: their Markov chain analysis and of the Qingbaikouan System in North China. Geological Bulletin regularly vertical stacking pattern in the third-order sequences. of China 26:249–255 (In Chinese with English abstract) Acta Geol Sin 75:421–431 Gao LZ, Zhang CH, Shi XY, Song B, Wang ZQ, Liu YM (2008a) Mobberley JM, Ortega MC, Foster JS (2012) Comparative microbial Mesoproterozoic age for Xiamaling Formation in North China diversity analyses of modern marine thrombolitic mats by plate indicated by zircon SHRIMP dating. Chin Sci Bull barcoded pyrosequencing. Environ Microbiol 14:82–100 53:2665–2671. doi:10.1007/s11434-008-0340-3 Monty CLV (1976) The origin and development of cryptalgal fabrics. Gao LZ, Zhang CH, Yin CY, Shi XY, Wang ZQ, Liu YM, Liu PJ, In: Walter MR (ed) Stromatolites: developments in sedimentol- Tang F, Song B (2008b) SHRIMP zircon ages: basis for refining ogy, vol 20. Elsevier, Amsterdam, pp 193–249 the chronostratigraphic classification of the Meso- and Neopro- Myshrall KL, Mobberley JM, Green SJ, Visscher PT, Havemann SA, terozoic strata in North China old land. Acta Geoscientica Sinica Reid RP, Foster JS (2010) Biogeochemical cycling and micro- 29:366–376 (In Chinese with English abstract) bial diversity in the thrombolitic microbialites of Highborne Cay, Gao LZ, Zhang CH, Liu PJ, Ding XZ, Wang ZQ, Zhang YJ (2009) Bahamas. Geobiology 8:337–354 Recognition of Meso- and Neoproterozoic stratigraphic frame- Niederberger M, Co¨lfen H (2006) Oriented attachment and meso- work in North and South China. Acta Geoscientica Sinica crystals: non-classical crystallization mechanisms based on 30:433–446 (In Chinese with English abstract) nanoparticle assembly. Phys Chem Chem Phys 8:3271–3287 123 Int J Earth Sci (Geol Rundsch) (2013) 102:401–413 413

Perri E, Spadafora A (2011) Evidence of microbial biomineralization Sprachta S, Camoin G, Golubic S, Le Campion Th (2001) Micro- in modern and ancient stromatolites. In: Seckbach J, Tewari V bialites in a modern lagoonal environment: nature and distribu- (eds) The Stromatolites: interaction of microbes with sediments: tion (Tikehau atoll, French Polynesia). Palaeogeogr Palaeoclim cellular origin, life in extreme habitats and astrobiology, vol 18. Palaeoecol 175:103–124 Springer, Berlin, pp 631–649 Su WB, Li HK, Huff WD, Ettensohn FR, Zhang SH, Zhou HY, Wan Perri E, Tucker ME (2007) Bacterial fossils and microbial dolomite in YS (2010) SHRIMP U-Pb dating for a K-bentonite bed in the Triassic stromatolites. Geology 35:207–210 Tieling Formation, North China. Chin Sci Bull 55:3312–3323 Perri E, Tucker ME, Spadafora A (2012) Carbonate organo-mineral Sumner DY, Grotzinger JP (1996) Were kinetics of Archean calcium micro- and ultrastructures in sub-fossil stromatolites: Marion carbonate precipitation related to oxygen concentration? Geol- lake, South Australia. Geobiology 10:105–117 ogy 24:119–122 Peryt TM, Hoppe A, Bechstaedt T, Koester J, Pierre C, Richter DK Sumner DY, Grotzinger JP (2000) Neoarchean aragonite precipita- (1990) Late Proterozoic aragonitic cement crusts, Bambui tion: Petrography, facies associations, and environmental signif- Group, Minas Gerais, Brazil. Sedimentology 37:279–286 icance. In: Grotzinger JP, James NP (eds) Carbonate Planavsky N, Ginsburg RN (2009) Thaponomy of modern marine sedimentation and diagenesis in the evolving Precambrian Bahamian microbialites. Palaios 24:5–24 world, vol 67. Society of Economic Paleontologists and Miner- Pruss SB, Corsetti FA, Fischer WW (2008) Seaﬂoor-precipitated alogists, Special Publication, Tulsa, Oklahoma, pp 123–144 carbonate fans in the Neoproterozoic Rainstorm member, Johnnie Sumner DY, Grotzinger JP (2004) Implications for Neoarchean ocean Formation, Death Valley Region, USA. Sediment Geol 207:34–40 chemistry from primary carbonate mineralogy of the Campbell- Qiao XF, Gao LZ, Zhang CH (2007) New idea of the Meso- and rand-Malmani platform, South Africa. Sedimentology 51:1273– Neoproterozoic chronostratigraphic chart and tectonic environ- 1299 ment in Sino-Korean Plate. Geol Bull Chin 26:503–509 Tang DJ, Shi XY, Pei YP, Jiang GQ, Zhao GS (2011) Redox status of Riding R (2008) Abiogenic, microbial and hybrid authigenic carbon- the Mesoproterozoic epeiric sea in North China. J Palaeogeogr ate crusts: components of Precambrian stromatolites. Geol Croat 13:563–580 (In Chinese with English abstract) 61:73–103 Thompson JB, Ferris FG, Smith DA (1990) Geomicrobiology and Riding R (2010) The nature of stromatolites: 3,500 million years of sedimentology of the mixolimnion and chemocline in Fayette- history and a century of research. In: Reitner J, Nadia-Vale´rie Q, ville Green Lake, New York. Palaios 5:52–75 Arp G (eds) Lecture Notes in Earth Sciences, vol 131. Springer, Turner EC, James NP, Narbonne GM (2000) Taphonomic control on Berlin, pp 29–74 microstructure in early Neoproterozoic reefal stromatolites and Sami TT, James NP (1994) Peritidal carbonate platform growth and thrombolites. Palaios 15:87–111 cyclicity in an early Proterozoic foreland basin, Upper Pethei Vasconcelos C, McKenzie JA, Bernasconi S, Grujic D, Tien AJ Group, northwest Canada. J Sediment Res 64:111–131 (1995) Microbial mediation as a possible mechanism for Sandberg P (1985) Aragonite cements and their occurrence in ancient dolomite formation. Nature 377:220–222 limestone. In: Schneidermann N, Harris PM (eds) Carbonate Walter MR, Heys GR (1985) Links between the rise of the metazoa cements, vol 36. SEPM, Special Publication, Tulsa, Oklahoma, and the decline of stromatolites. Precamb Res 29:149–174 pp 33–57 Wang HZ, Shi XY, Wang XL, Yin HF, Qiao XF, Liu BP, Li ST, Chen Shapiro RS, Awramik SM (2006) Favosamaceria cooperi new group JQ (2000) Research on the sequence stratigraphy of China. and form: a widely dispersed, time-restricted thrombolite. Guangdong Science and Technology Press, Guangzhou (In J Paleontol 80:411–422 Chinese) Shi XY, Zhang CH, Jiang GQ, Liu J, Wang Y, Liu DB (2008) Warthmann R, van Lith Y, Vasconcelos C, McKenzie JA, Karpoff Microbial mats in the Mesoproterozoic carbonates of the north AM (2000) Bacterially induced dolomite precipitation in anoxic China Platform and their potential for hydrocarbon generation. culture experiments. Geology 28:1091–1094 J Chi Uni Geosci 19:549–566 Young JD, Martel J (2010) The rise and fall of nanobacteria. Sci Am Soudry D, Weissbrod T (1995) Morphogenesis and facies relation- 302:52–59 ships of thrombolites and siliciclastic stromatolites in a Cam- Zhou HR, Mei MX, Du BM, Luo ZQ, Lu¨ M (2006) Study on the brian tidal sequence (Elat Area, Southern Israel). Palaeogeogr sedimentary features of high frequency Cyclothems of the Palaeoclim Palaeoecol 114:339–355 Wumishan Formation at Jixian, Tianjin. Geoscience 20:209–215 Spadafora A, Perri E, McKenzie JA, Vasconcelos C (2010) Microbial (In Chinese with English abstract) biomineralization processes forming modern Ca: Mg carbonate stromatolites. Sedimentology 57:27–40

123