One-billion-year-old eukaryotic algal fossil Arctacellularia from North China and its implications for the evolution of pre-Cryogenian filamentous multicellularity

Pre-Cryogenian organic-walled microfossils with delicate cellular preservation can provide pivotal information for the origin and early evolution of multicellular eukaryotes. With previously reported evidence for true dichotomous branching and photosynthesis, the filamentous fossil Arctacellularia is among one of the few examples of pre-Cryogenian unambiguous multicellular algae. However, the taxonomic diversity of this genus has remained controversial for decades, and its evolutionary implications for understanding the emergence and maintenance of filamentous multicellularity and branching in eukaryotes have been underexplored. Here, we report well-preserved Arctacellularia fossils extracted from the drill core samples of the early Tonian Liulaobei Formation (∼0.95–0.92 Ga), Huainan region, northern Anhui Province, North China. Two species have been recognized in the Liulaobei Formation, including the type species Arctacellularia tetragonala, with one trichome showing evidence of a possible nodal cell indicative of branching, and Arctacellularia ellipsoidea, distinguished by the presence/absence of barrel-like to long cylindrical cells (with a length/width ratio ≥ 1.5). Arctacellularia is reconstructed as a uniserial multicellular filamentous organism enveloped by common membrane in this study; it consists of three types of possibly differentiated cells that are characterized by terminal folds (or terminal extensions), and can occasionally bifurcate once via a nodal cell. This study suggests that the maintenance of filamentous multicellularity of Arctacellularia is achieved by a combination of common membrane, terminal folds, and siphonous construction. Furthermore, the dichotomous branching of Arctacellularia appears morphologically more primitive than those observed in other Pre-Cryogenian fossils, including Cheilofilum, Jacutianema, and Proterocladus. Given that Arctacellularia has been phylogenetically placed in the total group of Archaeplastida and the oldest Arctacellularia specimens date back to ∼1.7–1.4 Ga, if the early Mesoproterozoic material is confirmed to be biologically congeneric with the early Tonian counterpart, it suggests that Archaeplastida may have acquired multicellularity, siphonous construction, cellular differentiation, and possibly branching at least 1.4 billion years ago.