Phylum Porifera Phylum Porifera

Precambrian Sponges with Cellular Structures
Chia-Wei Li,* Jun-Yuan Chen,* Tzu-En Hua
Sponge remains have been identified in the Early Vendian Doushantuo phosphate deposit
in central Guizhou (South China), which has an age of 580 million years ago. Their
skeletons consist of siliceous, monaxonal spicules. All are referred to as the Porifera,
class Demospongiae. Preserved soft tissues include the epidermis, porocytes, amoebocytes,
sclerocytes, and spongocoel. Among thousands of metazoan embryos is a
parenchymella-type of sponge larvae having a shoe-shaped morphology and dense
peripheral flagella. The presence of possible amphiblastula larva suggests that the
calcareous sponges may have an extended history in the Late Precambrian. The fauna
indicates that animals lived 40 to 50 million years before the Cambrian Explosion.
REPORTS
Precambrian Sponges with
AnimalsCellular appear in theStructures
fossil record about poorly preserved to be clearly identified or
complex and is composed principally of
565 million years ago (Ma) in Vendian tillite. The were Nantuo shown Formation not toisbe dated sponges from (11). Some
Chia-Wei Li,* Jun-Yuan rocks Chen,* of the uppermost Tzu-En Hua Proterozoic (1), 620 a todisc-shaped 590 Ma. Theimpressions overlying Doushantuo
Formation lia haveisbeen of early reported Vendian as sponges, age, but this
from South Austra-
time known as the Ediacaran. Most of the
Ediacaran fossils are architecturally simple 590 Ma interpretation its base to 565 remains Ma at controversial its top. (11).
It is represented by a phosphate-dolostone
Sponge remains have been identified in the casts Early and Vendian molds, Doushantuo and none ofphosphate them can be deposit
in central Guizhou (South China), which associated has an age without of 580 question milliontoyears extant ago. phyla Their thick and have consists beenmainly from the of dark lowest phos-skeletal fossil
The earliest unequivocal sponge spicules
sequence in Wengan, where it is 33 to 55 m
skeletons consist of siliceous, monaxonal (2). spicules. It is uncertain All are referred whether to as the the Ediacaran Porifera, phate, cherty horizonphosphate, in Mongolia chert, (12) and of gray Late Ediacaran
class Demospongiae. Preserved soft tissues fauna include was the spark epidermis, of biological porocytes, diversity amoebocytes,
sclerocytes, and spongocoel. Among that ignited thousands the following of metazoan Cambrian embryos explo-
is taining a theIn uppermost Wengan rocks andofadjacent the Neopro-
parts of central
dolomite. age, The dated Dengying at 543 Formation, to 549 Ma con-(13)terozoic,
is a 180-m-thick dolomite sequence.
It is Ediacaran in age, ranging from
parenchymella-type of sponge larvae having sion a(1) shoe-shaped or was an evolutional morphologyexperiment
and dense Guizhou, late Proterozoic sedimentary rocks
peripheral flagella. The presence of possible that amphiblastula ended in extinction larva suggests (3). However, that 565 the Ma areatrepresented its base and 544 byMa the at its Nantuo, top. Doushantuo,
phosphate and Dengyin bed of Wengan formations con-
(14). The
calcareous sponges may have an extendedboth history comparative in the Late work Precambrian. on hemoglobin The fauna (4) The dark
indicates that animals lived 40 to 50 millionand years calibrated beforerates the Cambrian of nucleotide Explosion. sequence tains a Nantuo well-preserved, Formation diverse (0 flora toassem-
blage including lowermost multicellular unit, uncomfortably thallophytes, overlies the
147 m thick), the
divergence (5) suggested that there was an
acritarchs,
middle
and cyanophytes
Proterozoic
(15). The
Banxi
associated
fauna assemblage, however, had not
extended period of metazoan diversification
metamorphic
that began earlier in the mid-Proterozoic, been recognized. The abundant globular
Animals appear in the fossil record about perhaps about 1 billion years ago. The metazoan embryos had been previously interpreted
as phytoplanktonic organisms
565 million years ago (Ma) in Vendian chance of finding the missing metazoan
rocks of the uppermost Proterozoic (1), a record in the half-billion year long Proterozoic
gap was considered to be almost impos-
Wengan on Beidaoshan, the Doushantuo
(16).
time known as the Ediacaran. Most of the
About 15 km west of the county town of
Ediacaran fossils are architecturally simple sible by some, because it was thought that Formation consists of three units: the Lower
casts and molds, and none of them can be any early animals would be “squishy little Phosphate unit (20 m thick), the Middle
associated without question to extant phyla larva-like things” that would never have Dolostone unit (3.7 m) and the Upper
(2). It is uncertain whether the Ediacaran
phosphate unit (15 m). We prepared thin
been tough enough to show up in the fossil
fauna was the spark of biological diversity
sections (30 m thick) from three rock
record (6). The recent finding of phosphatized
metazoan embryos from basal Cam-
of Lower Phosphate unit. We identified 35
samples of a dark phosphate bed at the top
that ignited the following Cambrian explosion
(1) or was an evolutional experiment brian rocks in China and Siberia (7) indicated,
however, that metazoan embryos are from a 160-cm 2 area of the slides. These
individual sponges with light microscopy
that ended in extinction (3). However,
both comparative work on hemoglobin (4)
sponges are mostly globular but a few are
probably not uncommon as fossils but have
and calibrated rates of nucleotide sequence
tubular (Fig. 1, A and B), and range in size
Phosphatized sponge been overlooked remains, because of their 580 minute mya
from 150 to 750 m. The skeletons consist
divergence (5) suggested that there was an size and nondescript morphology. Here, we exclusively of thin monaxonal spicules that
extended period
40-50
of metazoanmy diversification
before describe an the assemblage Cambrian
of well-preserved are randomly dispersed in the mesohyl (Fig.
that began earlier in the mid-Proterozoic, sponge fossils from the Doushantuo phosphate
deposit (central Guizhou, China) of
1, A, B, D, and F). The spicules survived
perhaps about 1 billion years ago. The
chemical treatment by 4N HCl (on two
chance of finding the missing metazoan
specimens for 20 min), indicating that they
Early Vendian age, 580 Ma (8). are siliceous (17). Most of the spicules are
record in the half-billion year long Proterozoic
gap was considered to be almost impos-
Sponges are the most primitive metazoans
and their presence in the late Protero-
long. The largest is 4 m in diameter and
0.5 to 1.0 m in diameter and 10 to 60 m
sible by some, because it was thought that
zoic has been expected by molecular and 100 m long.
any early animals would be “squishy little
Analysis of the rocks and preservation of
morphological phylogenies (9). Occurrences
of the late Proterozoic (Ediacaran age)
larva-like things” that would never have
the Wengan fossils suggests that the sponges
were buried alive by catastrophic sedi-
been tough enough to show up in the fossil
sponge spicules have been reported previously
(10); however, many were either too
ment
Fig.
incursions.
1. (A)
Phosphate
A possible
alternation
longitudinal
preserveddispersed
the morphological monaxonal details spicules of the (s) softin the mesohyl (m). Two spicules firmly associated with spicule-
section of a tubular phosphatized sponge, showing the randomly
record (6). The recent finding of phosphatized
metazoan embryos from basal Cambrian
rocks in China and Siberia (7) indi-
C.-W. Li and T.-E. Hua, Department of Life Science, sponges, (B) including A phosphatized the epidermis, globular porocytes, sponge in a siliceous background (si); s, spicule. Scale bar, 50 m. (C)
tissues. producing Characteristic cells, the structures scleocytes, of living are encircled and enlarged in (E). so, spongocoel. Scale bar, 100 m.
cated, however, that metazoan embryos are National Tsing Hua University, Hsinchu, Taiwan, China. amoebocytes, Plasmolyzed sclerocytes, epidermal and cells spongocoel, (e) with nuclei (n). The epidermal cell in the square is magnified and is
J.-Y. Chen, Nanjing Institute of Geology and Palaeontology,
Academia Sinica, Nanjing, China.
Many(s) of in the(A). flatScale polygonal bar, epidermal 20 m. (E) cells Amoebocytes (a) in the mesohyl (m). Scale bar, 30 m. (F) Two
probably not uncommon as fossils but have
can be focused seen in athe different Doushantuo plane (insert); sponges. p, porocyte. Scale bar, 30 m. (D) High magnification of the spicules
been overlooked because of their minute
*To whom correspondence should be addressed. have their sclerocytes cytoplasmic (sc) with contents their and developing nuclei spicules (s); pm, plasma membrane. Scale bar, 10 m.
size and nondescript morphology. Here, we
preserved (Fig. 1C). Dense granules surrounding
the nucleus are probably cytoplas-
describe an assemblage of well-preserved
Fig. 2. (A) Spongocoel(so)withundigesteddebris.m,mesohyl;s,spicule.Scalebar,50m. (B–D) www.sciencemag.org
sponge fossils from the Doushantuo phosphate
deposit are framed) (central with yolkGuizhou, granules (y). China) Scale bar, of 50 m. (C and D) Embryosattheblastulastage.Scale
mic organelles. Scattered SCIENCE
among the VOL.
epidermal
cells are porocytes that form incurrent
279 6 FEBRUARY 1998 879
Embryos with uncertain affinities. (B) Ayoungmorula,showingsphericalblastomeres(twoofthem
pores (Fig. 1C). In the mesohyl, amoebocytes
with a variety of shapes were seen
Early Vendian bar, 50 m. age, (E) 580 Aprobablelongitudinalsectionofaparenchymellalarva(pa)withdistinctperipheral
Ma (8).
flagella (f). Flagella in the frame is magnified (insert). Scale bar, 50 m. (F )Abrokenspecimenwhich
Sponges mightare represent the most half ofprimitive an amphiblastula Phylum
metazoans
and is their connected presence to its parent in the (p) late by a curved Protero-
stalk (st); s, spicule. Scale bar, 50 m.
imens, six spicules were closely associated
larva (aa); e, epithelial cell. ScalePorifera
bar, 50 m. (G) Abud(b) (Fig. 1E). In one of the best preserved speczoic
has been expected by molecular and
morphological 880 phylogenies (9). Occurrences
of the late Proterozoic (Ediacaran age)
SCIENCE VOL. 279 6 FEBRUARY 1998 www.sciencemag.org
sponge spicules have Or been: reported What previously
(10); however, many were either too
Fig. are 1. (A) A possible Sponges longitudinal section of Anyway?
a tubular phosphatized sponge, showing the randomly
dispersed monaxonal spicules (s) in the mesohyl (m). Two spicules firmly associated with spiculeproducing
cells, the scleocytes, are encircled and enlarged in (E). so, spongocoel. Scale bar, 100 m.
C.-W. Li and T.-E. Hua, Department of Life Science, (B) A phosphatized globular sponge in a siliceous background (si); s, spicule. Scale bar, 50 m. (C)
National Tsing Hua University, Hsinchu, Taiwan, China. Plasmolyzed epidermal cells (e) with nuclei (n). The epidermal cell in the square is magnified and is
J.-Y. Chen, Nanjing Institute of Geology and Palaeontology,
Academia Sinica, Nanjing, China.
(s) in (A). Scale bar, 20 m. (E) Amoebocytes (a) in the mesohyl (m). Scale bar, 30 m. (F) Two
focused in a different plane (insert); p, porocyte. Scale bar, 30 m. (D) High magnification of the spicules
*To whom correspondence should be addressed. sclerocytes (sc) with their developing spicules (s); pm, plasma membrane. Scale bar, 10 m.
www.sciencemag.org SCIENCE VOL. 279 6 FEBRUARY 1998 879
REPORTS
poorly preserved to be clearly identified or
were shown not to be sponges (11). Some
disc-shaped impressions from South Australia
have been reported as sponges, but this
interpretation remains controversial (11).
The earliest unequivocal sponge spicules
have been from the lowest skeletal fossil
horizon in Mongolia (12) of Late Ediacaran
age, dated at 543 to 549 Ma (13).
In Wengan and adjacent parts of central
Guizhou, late Proterozoic sedimentary rocks
are represented by the Nantuo, Doushantuo,
and Dengyin formations (14). The
Nantuo Formation (0 to 147 m thick), the
lowermost unit, uncomfortably overlies the
middle Proterozoic Banxi metamorphic
Phylum Porifera
-- 5000 -10000 spp.
-- mostly marine some fw
none terrestrial
-- 3 classes, most important
distinction are skeletal
characteristics
Phylum Porifera
I. General Ecological Characteristics
II. Body Plan
III. Metazoan Characteristics
A. Cell types
B. Allorecognition
C. Reproduction and Embryology
D. Other metazoan homologies.
IV. Sponge Phylogeny
I. General Ecological Characteristics
Sponges are:
• Sessile, benthic
• Filter feeders
• Competitors for space
• Fed upon by specialist predators
• Grow in many forms, solitary,
colonial, branching, as thin
sheets over substrates
• From few cm to over 1 m in size
• Estimated in some cases to be
several hundred years old
II. General Characteristics of
the Poriferan Body Plan
3 major types of body construction
Asconoid
Syconoid
Leuconoid
(this has little to do with the
classification of sponges, which is
based on skeletal morphology)
1

Osculum
Asconoid Sponge
Syconoid Sponge
Ostia
Leuconoid Arrangement
These are the largest, and most sponges
have this type of construction
Carnivorous
sponges from deep
water and shallow
caves
Evolution of
macrophagy from a
microphagous,
filter feeding life
style
Kinship between sponges and protistans?
Further supported by
choanoflagellate vs. choanocyte similarity
II. Other Characteristics of
the Poriferan Body Plan
No true muscular system
Lacking sensory organs, nervous system
Often amorphous and asymmetrical,
no anterior, posterior, oral surfaces
Begs the question: Colony of protista or
a simple metazoan (i.e. an integrated animal ?)
2

What is a Metazoan?
III. Metazoan-like Characteristics of Sponges
A. 5 different principal cell types (20 total)
In other words what are the inherent
characteristics of an animal body plan that
are different from that of a colonial
heterotrophic organism?
Choanocyte
spongocoel
Osculum
Pinacocyte
Porocyte
Sclerocytes
Archeocyte
http://www.biology.ualberta.ca/facilities/multimedia/uploads/zoology/Porifera.swf
Stem cells – have the capacity of self-replication
and to give rise to more than one type of
mature daughter cells
III. Metazoan-like Characteristics of Sponges
B. Complex reproduction
Image courtesy of BioMEDIA ASSOCIATES
Archeocytes – in sponge embryos are considered
totipotent stem cells that can give rise to an
entire organism
- in adults they produce a few cell types
(sclerocytes, germ cells, etc.) but not an
entire organism; they are considered
pluripotent
Muller (2006) Seminars in Cell and Developmental Biology #17:481-491
III. Metazoan-like Characteristics of Sponges
B. Complex reproduction
III. Metazoan-like Characteristics of Sponges
Unique but complex embryonic development, with a hollow
blastula stage but does not form a gastrula
sperm
Egg
Carried in the plankton
Parenchymula or
Amphiblastula
Juvenile
Settlement &
metamorphosis
Adult
Sexual reproduction involves fertilization, release of a planktonic
larva, and its eventual settlement and metamorphosis on the bottom.
3

III. Metazoan-like Characteristics of Sponges
C. Other sponge metazoan homologies: Epithelium
-- epithelial-like layer homologous to animal epithelia
( ...but typically basal lamina only in Homoscleromorphs)
-- septate junctions (desmosomes) albeit primitive and small
(only Calcarea has full “animal-like” desmosomes)
-- extracellular matrix
-- spongin is collagen-like molecule
-- ubiquitin protein similarity (tag other proteins
for proteolysis)
III. Metazoan-like Characteristics of Sponges
C. Other sponge metazoan homologies:
Regulation of Development
-- True Hox genese are not found, but many homologous
developmental transcription factors are conserved
-- Most of the developmental signaling pathways
(Wnt, Notch) and they are expressed along the same
embryonic “axis” in sponges (and Cnidaria).
Many of these signaling pathways and transcription
factors have not been found in Protists.
From Adamaska et al., 2011
III. Metazoan-like Characteristics of Sponges
B. Non-self recognition
“Metazoan-like Characteristics of Sponges”
Allorecognition
Histoincompatability
“Allorecognition”
Some sponges form new individuals hours after their
cells are separated from one another. If species are
combined, the cells segregate with their own
“Metazoan-like Characteristics of Sponges”
Allorecognition
Histoincompatability
Summary
-- Sponges lack complexity, but their body plan is
ecologically and evolutionarily successful
--They should be considered metazoans
since they have fundamental characteristics of
multicellular animals;
Immune response:
antagonism toward foreign substances
antagonism must be specific toward that substance
future responses should be altered by the first response
--They are derived from flagellated protists but may be a
early and now distant branch of the metazoa;
animals are monophyletic
The sponge immune response is mediated by molecules which have
been found to control histo-recognition in deuterostomes
including Immunoglobulin-like domains and citokines
4

Phylum Placozoa
-- 2-3 mm, 25 um- thick, resembling a large ameba
-- Lacks anterior posterior polarity
-- Asexual reproduction is prevalent
--The most primitive animal?
Phylum Placozoa
epithelium-like layer
Fiber synctium
Dorsal
cilium
thick glandular layer
Flagellated cells
Intercellular
junctions
- - Feed ventrally by absorption of digested material
- - Lack organs but tissue-like outer walls (no basement membrane)
- - A bit more than 2000 cells
- - Only 4 different cell types (20 in sponges; > 220 in mammals)
- - Smallest genome of all animals
Trichoplax adhaerens
Three competing Scenarios
A. Earliest view of them as the basal metazoan
B. Special cellular junctions consisting of two opposing
dense plaques (desmosomes) not found in most sponges
C. 16S rRNA data…maybe secondarily simplified from more
complex ancestors?
Mitochondrial genome of
Trichoplax adhaerens
supports Placozoa as the
basal lower metazoan phylum
Dellaporta, Stephen L.
et al. (2006) Proc. Natl.
Acad. Sci. USA 103,
8751-8756
Largest known mt genome 46
kbp, 2x that of most metazoa
with introns and other
intrageneic spacers and large
protein coding regions that are
usually lacking in other animals
Blue: known mt proteins
Gray: ribosomal genes
Green: unknown open reading frames
Red lines: introns
(a sponge)
Conclusions?
5