Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite

Abstract

Phosphorites of the late Neoproterozoic (570 Ϯ 20 Myr BP) Doushantuo Formation, southern China, preserve an exceptional record of multicellular life from just before the Ediacaran radiation of macroscopic animals. Abundant thalli with cellular structures preserved in three-dimensional detail show that latest-Proterozoic algae already possessed many of the anatomical and reproductive features seen in the modern marine flora. Embryos preserved in early cleavage stages indicate that the divergence of lineages leading to bilaterians may have occurred well before their macroscopic traces or body fossils appear in the geological record. Discovery of these fossils shows that the early evolution of multicellular organisms is amenable to direct palaeontological inquiry.Most of the fossils that document the first 85% of evolutionary history are microscopic. Not until the Phanerozoic eon (Ͻ544 Myr BP) do the remains of large animals, algae and, later, plants become conspicuous constituents of the sedimentary record. The most important biological event that connects these palaeobiologically distinct eras is the evolution of complex multicellularity in eukaryotes. Multicellular organisms arose at least six times: in animals, fungi and several groups of algae 1 . Macroscopic remains of uncertain systematic affinities occur in rocks as old as 1,800-2,100 Myr BP 2 and cellularly preserved microfossils of red, green and stramenopile (brown and related) algae indicate that multicellularity was achieved in these groups by about 1,000 Myr 3 . Multicellularity may have evolved comparably early in minute ancestral animals, but until now any pre-Ediacaran animal history has been contentious and thought by many to be unrecognized and perhaps unrecognizable by palaeontologists.Phosphorites of the Doushantuo Formation in southern China contain three-dimensionally preserved fossils that record in exquisite Figure 1 Location and generalized stratigraphy of the fossiliferous Weng'an section in Guizhou Province, South China. The arrow indicates the principal stratigraphic horizon containing phosphatized algae and embryos. Fm, Formation.Figure 2 Algal thalli from the Doushantuo phosphorite and the modern bangiophyte red alga, Prophyra suborbiculata. a-c, Thalli from Doushantuo phosphorite. a, b, Scanning electron micrographs of a thallus composed of cuboidal cell packets similar to those of modern chlorosarcinacean green algae; b, the upper left quadrant of a at higher magnification. c, Photomicrograph of cruciate cell tetrads embedded in a foliose thallus; d, Carposporangia within the thallus of living Porphyra. Scale bar (in d): 200 m for a; 50 m for b; and 100 m for c and d.

Laser‐Raman and atomic force microscopy assessment of the chlorococcalean affinity of problematic microfossils

“…We are aware that our findings have also bearing on the ongoing discussion concerning the biological affinities of phosphatic microfossils from the Neoproterozoic (Ediacaran) Doushantuo Formation of south China described originally as post mortem phosphatized volvocalean-like green algae [44,45] or resting eggs and blastula embryos of early animals 8 [46,47,48,49,50] . Interestingly, these microfossils have recently been also interpreted as remnants of giant bacteria comparable to modern sulphur bacteria of the genus Thiomargarita [51,52] .…”

“…This conclusion confirmed our earlier suggestion [4] that many acritarchs are unicellular green algae and that the internal bodies represent their asexual reproductive structures (spores). To our knowledge, the c. 420 Ma-old specimens shown in this report represent the earliest thus far described sporulating unicellular green algae (Chlorococcales).We are aware that our findings have also bearing on the ongoing discussion concerning the biological affinities of phosphatic microfossils from the Neoproterozoic (Ediacaran) Doushantuo Formation of south China described originally as post mortem phosphatized volvocalean-like green algae [44,45] or resting eggs and blastula embryos of early animals 8 [46,47,48,49,50] . Interestingly, these microfossils have recently been also interpreted as remnants of giant bacteria comparable to modern sulphur bacteria of the genus Thiomargarita [51,52] .…”

Affinity, life cycle, and intracellular complexity of organic-walled microfossils from the Mesoproterozoic of Shanxi, China

“…Term acritarchs, which was applied to such organisms in referring to their uncertain origins, is now somewhat misleading because many of these microfossils have been progressively allocated to specific groupings, mainly eukaryotic phytoplankton (Tappan, 1980;Moczydłowska, 1991Moczydłowska, , 2011Colbath and Grenfell, 1995;Arouri et al, 1999Arouri et al, , 2000Talyzina and Moczydłowska, 2000;Wicander, 2002;Grey, 2005;Traverse, 2007;Molyneux, 2009;Kaźmierczak and Kremer, 2009;Moczydłowska et al, 2011). There are exceptions, such as microfossil Tianzhushania identified as a metazoan embryo (Xiao et al, 1998;Yin et al, 2004Yin et al, , 2007 or a holozoan protist (Huldtgren et al, 2011;Bengtson et al, 2012), and "Tappania" from the Wynniatt Formation as a fungus (Butterfield, 2005(Butterfield, , 2009Javaux 2007). Some unidentified Ediacaran taxa, together with Alicesphaeridium and Gyalosphaeridium, were claimed to be potential diapause egg cysts (Cohen et al, 2009), based on morphology but lacking the evidence of cell division (Moczydłowska et al, 2011).…”

Hbox1 and Hbox7 are involved in pattern formation in sea urchin embryos

“…In Drosophila, genetic analyses have demonstrated that homeobox genes control embryonic segment number, polarity and identity (Akam 1987;Scott & Carroll 1987). The fossils of embryos identified in a Precambrian phosphate deposit in central Guizhou show that the body plans of these prototypes of bilateral eumetazoa are similar to those of extant marine invertebrate embryos (Xiao et al 1998). It has been suggested that marine invertebrate embryos inherited the original bilaterian body plan (Davidson et al 1995).…”