Diversification of heterotrophic protists at the eve of Cambrian explosion

Highlights

• Two new types of foraminifera from the Gaojiashan Member, Dengying Formation of the terminal Neoproterozoic.

• A hollow pear-shaped structure with long extending, a solid spindle-shaped structure with straight narrow central tube.

• The assemblage of protists increase the global diversification of protists in the latest Ediacaran.

• The global distributions of Radiolaria, foraminifera and VSMs from the Neoproterozoic to the Cambrian are summarized.

• Typical representatives of heterotrophic protists are selected from the Neoproterozoic to the Cambrian.

Abstract

Molecular clocks suggest that at least some heterotrophic protists, such as foraminifera, testate amoebae and tintinnids, were present in ecosystems as far back as 1000 Ma. Vase-shaped microfossils of earlier testate amoebae from the supergroups Amoebozoa and Rhizaria occur globally in pre-Sturtian shallow marine deposits, and have thus been considered as a potential biostratigraphic tool, especially at a time span between 789 and 729 Ma. Organic-rich three-dimensional tests having flask-like shapes, constricted necks, distinct and often thickened collars of possible tintinnids affinity were recovered from 715 to 635 Ma carbonate deposits from the Tsagaan Oloom Formation, southwestern Mongolia. Phosphatic scaly structures of unknown affinity were reported from mid-Neoproterozoic (pre-Sturtian) strata of northwest Canada. Anyhow, the fossil records of heterotrophic protists aftermath the Cryogenian age are still shroud in mist. The three putative ciliate fossils, namely Eotintinnopsis, Wujiangella, and Yonyangella from the Neoproterozoic Doushantuo Formation in China were reassessed and likely to be taphonomically and diagenetically distorted and altered acritarchs. Here, we report a diverse assemblage of problematic from the terminal Ediacaran Gaojiashan biota in southern Shaanxi Province, China. Apart from the renowned vase-shaped Protolagena and Sicylagena, likely thought to be the earliest foraminifera, new findings include a hollow pear-shaped structure with long extending, a solid spindle-shaped structure with straight narrow central tube. Possible foraminifera from the Gaojiashan biota may throw welcome new light to the long obscured history of heterotrophic protists at the eve of the Cambrian explosion.

Introduction

Marine protists consist of phototrophic and heterotrophic unicells with a wide cell size ranges (Ohtsuka et al., 2015) and are regarded as categories of eukaryotic microbes that contain all eukaryotes except plants, animals and fungi (O'Malley et al., 2013). Protists account for the enormous majority of eukaryotic life today, representing the major lineages and an evolutionary history far outdistance that of animals, plants and fungi. In addition, eukaryotes might independently be derived from different protistan ancestors (O'Malley et al., 2013). Hence, Protists play noticeable important roles in understanding eukaryotic life on Earth (O'Malley et al., 2013).

The fossil record of the early eukaryotes including marine protists is continual updated (Porter, 2004, 2006; Javaux, 2007, Javaux, 2011; Blank, 2013; Knoll, 2014). The oldest marine protist microfossil recovered is an acritarch from the shales and silty shales of the 1.8-Ga Changzhougou Formation, the lowermost Changcheng Group in the Pangjiapu Region of North China (Lamb et al., 2009). The fossil records of calcareous nannofossils, diatoms and dinoflagellates are vitally beneficial for reconstruction of primary productivity in the geological history (Ohtsuka et al., 2015). In spite of this, dominant heterotrophic protists such as ciliates are considered nearly completely missing in the fossil records (Ohtsuka et al., 2015). Due to the inadequate preservation and paleontological evidence, foraminifera are long thought to emerge in the early Cambrian (McIlroy et al., 2001; Pawlowski et al., 2003; Streng et al., 2005).

However, with more fossil materials identified and biomarker evidence as a tool, fossil record of heterotrophic protists is gradually increased during the Neoproterozoic when modern eukaryotes are supposed to originate (Bosak et al., 2011a, Bosak et al., 2011b). Based on the molecular clocks research, a eukaryotic group including ciliates, dinoflagellates, and apicomplexans diverged at 1360–950 Ma (Douzery et al., 2004; Berney and Pawlowski, 2006) and ciliates diverged at 776 ± 92 Ma (Douzery et al., 2004) or after 500 Ma (Berney and Pawlowski, 2006). Though the oldest ciliates reported in the late Ediacaran phosphorites of the Doushantuo Formation in China (Li et al., 2007) was reinterpretated as diagenetically and taphonomically distorted and altered acritarchs (Dunthorn et al., 2010), exceptionally preserved 715–635 m.y. old putative ciliates with flask-like shapes, constricted necks, extended the stratigraphic range of ciliate body fossils by >100 m.y (Bosak et al., 2011b), which filled the gap of the sparse record of eukaryotes between the Sturtian and Marinoan glaciations, although the Sturtian dramatic environment change made fossil record limited between these two glaciations (Knoll et al., 2006). In addition, vase-shaped fossil testate amoebae from the Rasthof Formation (746 ± 2–635.6 ± 0.5 Ma) of the Congo craton in northern Namibia and the Tsagaan Oloom Formation (773.5 ± 6.6–635 Ma) of the Dzabkhan terrane in Mongolia in the carbonates that cap glacial strata provide evidence of thriving subtidal ecosystems in the aftermath of the Sturtian glaciation (Bosak et al., 2011a). What's more, very large vase-shaped microfossils from carbonate nodules of the upper Chuar Group (Porter and Knoll, 2000) are identified as testate amoebae related to foraminifers. The agglutinated tubular microfossils interpreted as early-diverging foraminifera from the Rasthof Formation, Namibia (715 Ma marine carbonates) predate the earliest undisputed occurrences of fossil foraminifera by ~150 m.y (Bosak et al., 2012). The scarceness of the early foraminiferal fossil record might reflect its poor preservation or incomplete sampling and investigation (Hua et al., 2010).

The Gaojiashan biota (548 ± 8 Ma) (Cui et al., 2016) from the south Shaanxi Province, China yields a vase-shaped microfossil assemblage of putative foraminifera, including two genera and five species, namely Protolagena limbata, P. gaojiashanensis, P. papillata, Sicylagena formosa and S. latistoma (Chai et al., 2020). Here we report a combination of new protists that extend the diversification of the heterotrophic protists after the Snowball Earth event and may add to the record of the ever-growing earliest calcareous foraminifera at the latest Ediacaran.