The Proterozoic macrofossil Tawuia as a posible siphonous macroalga

1. The Proterozoic macrofossil Tawuia as a possible siphonous macroalga
Qing Tang1*, Ke Pang2,3, Lei Chen4, Guangjin Li4, Xunlai Yuan2,3, and Shuhai Xiao5
1Department of Earth Sciences, University of Hong Kong, Pokfulam Road, Hong Kong, China; 2State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and
Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing, 210008; 3University of Chinese Academy of Sciences, Beijing 100039, China;
4College of Earth Science and Engineering, Shandong University of Science and Technology, Qingdao 266590, China; 5Department of Geosciences and Global Change Center, Virginia Tech,
Blacksburg, Virginia 24061, USA; *qingt@hku.hk
1. Introduction
When and how macroscopic (>1 mm in size) algae (photosynthetic
eukaryotes) evolved in the Earth has been hotly debated. This is
largely because the Proterozoic macrofossils are usually
morphologically simple and phylogenetically uncertain. The
sausage-like carbonaceous macrofossil Tawuia, for
example, is ubiquitous in Proterozoic successions (Fig. 1).
However, the phylogenetic interpretation of Tawuia
remains elusive, hampering our understanding of its
evolutionary significance in early eukaryotes. Our study reports
exceptionally preserved Tawuia specimens from the Tonian
(1.0 to 0.72 Ga) successions in North China. The new
materials show that Tawuia is a tomaculate organism,
sometimes with an axial stripe, terminal discoidal structures,
and transverse constrictions, indicating that Tawuia is
probably a coenocytic macroalga. Given the earliest fossil
record of Tawuia as much as 1.6 Ga old, the new data
provide important constraints on the origin and early evolution of
coenocytic eukaryotes, primary plastids, and macroalgae.
Major object:
• Understand the taphonomy and biology of Tawuia and its
evolutionary significance in early eukaryotes.
Figure 1. General morphology and known stratigraphic range of Tawuia.
1 mm
Tawuia
1.6 Ga 0.55 Ga

2. 2. Material
• A total of 363 specimens of Tawuia preserved
in carbonaceous compression and pyritization
were collected from the Tonian
Shiwangzhuang Formation in Shandong
Province and the Liulaobei Formation in
Anhui Province, North China (Fig. 2).
Figure 2. Geological map (A) and stratigraphic columns (B) of the Proterozoic sequences in the western Shandong
Province and Anhui Province, North China. Vertical purple bars indicate stratigraphic occurrences of Tawuia
specimens examined in this study. Modified from Tang et al. (2021).
3. Method
• Reflected light microscopy were used to
observe general morphology of Tawuia
specimens.
• Backscattered electron scanning electron
microscopy (BSE-SEM) and energy dispersive
X-ray spectroscopy (EDS) were used to
characterize microstructures and chemical
compositions of pyritized specimens.

3. 4. Results
• Tawuia vesicles vary from I-, C-, S-, U-, L-
, to dumbbell-shaped in general
morphology usually with concentric
folds at termini and longitudinal folds in
the central part (Fig. 3).
• Some specimens have a distinct
transverse constriction that
asymmetrically divides the tomaculate
vesicle into two unequal parts (Fig. 4A).
• A large discoidal structure is present at
one or both termini of some Tawuia
specimens (Fig. 4B-C).
• Occasionally, some specimens preserve
an elongate axial stripe whose shape is
consistent with the morphology of
hosting vesicle (Fig. 5A-D).
• BSE-SEM and EDS analyses of a rusty
specimen show that the rusty axial
stripe is filled with euhedral pyrites and
is covered under black carbonaceous
remains of the vesicle (Fig. 5E-L).
Figure 3. Various morphologies of Tawuia vesicles. Figure 4. Asymmetrical constrictions (yellow arrowhead) and
terminal discs (white arrowhead) in Tawuia vesicles
Figure 5. Axial stripes in Tawuia vesicles. Yellow arrowheads in A–D denote dark axial stripes; cyan arrows in E denote rusty
axial stripe covered with fragments of carbonaceous material (white arrowheads); cyan arrowhead in F and H denotes
euhedral pyrite; and black arrowheads in F and G denote carbonaceous material of vesicle wall.

4. 5. Discussion
• The concentric and longitudinal folds suggest
that Tawuia was originally cylindrical with two
hemispheric termini.
• The transverse constrictions and terminal discs
in some Tawuia specimens are interpreted as
biological structures and they indicate the
presence of a multicellular stage in the life
cycle of Tawuia.
• The axial stripes in Tawuia vesicles may
represent condensed and consolidated
eukaryotic protoplasts during encystments,
programmed cell death, or even cell
degradation (Fig. 6), suggesting that Tawuia
vesicles likely represent giant cells with a
recalcitrant cell wall.
• Thus, given the millimeter-centimeter vesicle
size, Tawuia is interpreted as a coenocytic
eukaryote and likely a macroalga.
Characters
Fossil Chlorophyta
Xanthophyt
a
Rhodophyt
a
Fungi Amoeba Bacteria
Tawuia
Valonia
ventricosa
Characiosip
hon
Vaucheria Griffithsia
Neurospora
aseptate
hyphae
Chaos Thiomargarita
sketch
unicell (vegetative stage) √ √ √ √ x √ √ x
coenocyte √ √ √ √ √ √ √ x
macroscopic size √ √ √ √ √ √ √ x
recalcitrant cell wall √ √ √ √ √ √ x √
tomaculate shape √ √ √ x x x x x
allometric growth √ √ √ √ √ √ x x
branch x x x √ √ √ x x
cyst and excystment √ (?) √ √ √ x √ √ √
holdfast/ rhizoid x √ √ √ √ √ x x
asymmetric constriction √ x x x x x x x
abscission structure √ x x x x x x x
Figure 6. Schematic diagram
showing the formation of
axial stripe in Tawuia
specimens.
Table 1. Morphological
comparison between
Tawuia and modern analogs
of eukaryotes and bacteria.
“√” denotes presence, “x”
denotes absence, “?”
denotes uncertainty. Cells
in yellow shading represent
similarities to Tawuia.
5.1 Morphological reconstruction

5. 6. Conclusions
• Our phylogenetic interpretation of
Tawuia as a coenocytic eukaryote and
a possible macroalga, provides an
important example of photosynthetic
eukaryotes during the time period of
1.7–1.0 Ga, and can be used to test
various molecular clocks estimates on
the origins of eukaryotes and primary
plastids (Fig. 7).
5.2 Evolutionary significance
• Our systematic analyses of exceptionally preserved fossils of Tawuia from the Tonian of North China revealed important characters such
as coenocytic cell construction, asymmetric constriction, abscission structures, and recalcitrant cell wall.
• Together, these characters indicate that Tawuia is likely a millimeter-sized coenocytic eukaryote and possibly a macroalga.
• Our study, if confirmed, indicates that photosynthetic eukaryotes may have attained macroscopic sizes through coenocytism ca. 1.6 Ga,
and by implication eukaryotes and primary plastids may have evolved before 1.6 Ga.
• The coenocytic cell construction of
Tawuia suggests macroscopic and
coenocytic eukaryotes may have
evolved in the early Mesoproterozoic.
Figure 7. Time calibrated phylogenetic tree of photosynthetic eukaryotes (algae), showing that the oldest known occurrence
of Tawuia at ca. 1.6 Ga is broadly consistent with the molecular clock estimate of algae in Paleo- to Mesoproterozoic. Modified
from Sanchez-Baracaldo et al. (2017).
oldest
occurrence
of
Tawuia
7. References
• Tang, Q., Pang, K., Li, G., Chen, L., Yuan, X., Sharma, M., Xiao, S., 2021. The Proterozoic macrofossil Tawuia as a coenocytic eukaryote and a possible macroalga. Palaeogeogr. Palaeoclimatol. Palaeoecol. 576, 110485.
• Sánchez-Baracaldo, P., Raven, J.A., Pisani, D., Knoll, A.H., 2017. Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc. Natl. Acad. Sci. U.S.A. 114, E7737–E7745.