Horodyskia, characterized by a string of beads with uniform size and spacing, represents one of few examples with a fossil record extending from the early Mesoproterozoic Era (~1.48 Ga) to the terminal Ediacaran Period (~550 Ma). Horodyskia also has a wide global distribution, but its biological affinity remains controversial.
The new specimens, from the Tonian Shiwangzhuang Formation (~850–720 Ma) in western Shandong and Jiuliqiao Formation (~950–720 Ma) in Huainan region, North China, are unique in their diverse preservational styles, including carbonaceous compressions, three-dimensionally preserved organic-walled fossils, shallow impressions, and casts and molds.
Horodyskia fossils provide evidence to illuminate their biogenicity. This study reports evidence that Horodyskia may have attained its macroscopic size through the combination of coenocytism and simple clonal coloniality.
The results were published on April 12, 2023, in Communications Biology, a professional journal in biology.
Proterozoic macroscopic fossils are crucial for our understanding of the early evolution of eukaryotes, particularly in terms of how and when early eukaryotes developed complex multicellular grades of organization and acquired body sizes that are visible to the naked eyes. However, fossils at the millimetric-centimetric scale are relatively scarce in successions older than the Neoproterozoic Era and their biogenicity and phylogenetic positions often remain contentious, hampering our ability to reconstruct the tempos and modes of early eukaryote evolution.
Various opinions concerning about the nature of Horodyskia have been proposed. One of the prominent features of Horodyskia in previously reported specimens is the cast-and-mold preservation in fine-grained siliciclastic rocks or in cherts (silicification), with no evidence for the preservation of organic walls. This feature further impedes the biological and phylogenetic interpretation of Horodyskia.
A team of scientists led by Dr. LI Guangjin and Research Prof. PANG Ke from Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGPAS), and Prof. CHEN Lei from Shandong University of Science and Technology, reported freshly excavated Horodyskia specimens They were observed and characterized using light microscopy (LM), scanning electron microscope (SEM) with both backscattered electron (BSE) and secondary electron (SE) detectors, Energy dispersive X-ray spectroscopy (EDS) elemental mapping, and Raman spectroscopy (see Methods).
The carbonaceous nature of Horodyskia fossils, similar to representative carbonaceous compression macrofossils from the Shiwangzhuang Formation, suggests an underlying biological origin. Importantly, the carbonaceous compression specimens and three-dimensionally preserved organic-walled specimens are similar in morphology and size, strongly disputing the possibilities of sedimentary structures, mud flocs, and intraclasts. Raman spectroscopy reveals that the carbonaceous material of the Shiwangzhuang Horodyskia specimens have spectral characteristics similar to co-existing multicellular fossils, indicating that they both experienced low-grade metamorphism with similar peak metamorphic temperatures. Given the presence of possible compressional folds and three-dimensional preservation, the Shiwangzhuang and Jiuliqiao specimens suggest that Horodyskia beads are bona fide fossils with organic-walled vesicles.
The Shiwangzhuang material provides a valuable link between the early Mesoproterozoic and late Ediacaran horodyskids (Horodyskia and Horodyskia-like fossils). Two groups of fossils with distinct bead sizes are observed on the same bedding plane in the Shiwangzhuang Formation. They have the same preservational style, exhibit similar positive correlations between bead diameter and spacing and between bead diameter and distance, and share a largely overlapping chemospace distribution, suggesting that they are not only biogenic, but also likely congeneric organisms. The ranges of their bead diameters overlap with that of Horodyskia minor from the Liuchapo Formation and that of H. moniliformis from the Appekunny Formation, respectively, supporting the assignment of specimens with sub-millimetric beads to the genus Horodyskia. Therefore, this study suggests that Horodyskia has a stratigraphic range from early Mesoproterozoic to late Ediacaran, with remarkable long-term morphological stability over 900 Myr.
Overall, Horodyskia can be reconstructed as a chain-like organism or a colony of individuals composed of several to dozens of vesicles or cells with a recalcitrant organic wall and likely embedded in amorphous gelatinous matrix. The observed division in beads and paired beads likely resulted from binary fission indicate that the sub-millimetric to millimetric beads of Horodyskia very likely represent giant cells. Horodyskia cells are orders of magnitude larger than typical prokaryotic cells, and their inferred recalcitrant cell walls with a large size are unusual for prokaryotic cells. Therefore, Horodyskia is unlikely to be a prokaryotic organism.
“The large cell size of Horodyskia indicates that it is not only a eukaryote, but also likely a multinucleated or coenocytic eukaryote,” PANG says, “the sub-millimeter- to millimeter-sized cells of Horodyskia seem to require multiple nuclei to regulate the giant mass of cytoplasm.”
The cellular nature and the unconnected but occasionally dividing feature of Horodyskia beads, indicate that these fossils are unlikely to be complex multicellular organisms, but are more likely to be protists whose clonal cells forming simple and not fully integrated colonies (simple clonal coloniality). Protists with a construction of simple clonal coloniality, a sub-millimetric to millimetric cell size (or inferred coenocyte), and a recalcitrant cell wall, features that define Horodyskia, are limited to a smaller number of eukaryotic clades. This study evaluated the three most likely potential analogs: arcellinid testate amoebae, foraminifers, and some algal groups, which are proposed in previous studies.
The most plausible phylogenetic interpretation for Horodyskia is that it represent a multicellular and giant-celled protist, which has acquired a large body size and shares some similarities with living coenocytic algae and monothalamid foraminifers, although the latter are typically unicellular and therefore less likely. Together with other possible early-middle Proterozoic coenocytic fossils, Horodyskia provides an important temporal constraint on the origin of coenocytic eukaryotes.
This research was supported by the National Key R&D Program of China, National Natural Science Foundation of China, Chinese Academy of Sciences, State Key Laboratory of Palaeobiology and Stratigraphy, Youth Innovation Promotion Association of CAS, China Postdoctoral Science Foundation and Taishan Scholars Project.
Reference: Li G, Chen L*, Pang K*, Tang Q, Wu C, Yuan X, Zhou C and Xiao S, 2023. Tonian carbonaceous compressions indicate that Horodyskia is one of the oldest multicellular and coenocytic macro-organisms. Communications Biology, 6: 399. https://doi.org/10.1038/s42003-023-04740-2.
Horodyskia moniliformis and Horodyskia minor from the Tonian Shiwangzhuang Formation. Most beads of H. moniliformis are enveloped in a halo.
Schematic reconstruction of Horodyskia moniliformis (larger beads) and Horodyskia minor (smaller beads).
Contact:
LIU Yun, Propagandist
Email: yunliu@nigpas.ac.cn
Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences
Nanjing, Jiangsu 210008, China
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