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Prospects & Overviews
Of early animals, anaerobic
mitochondria, and a modern sponge
Marek Mentel1), Mayo Röttger2), Sally Leys3), Aloysius G. M. Tielens4)5)
and William F. Martin2)
The origin and early evolution of animals marks an
important event in life’s history. This event is historically
associated with an important variable in Earth history oxygen. One view has it that an increase in oceanic
oxygen levels at the end of the Neoproterozoic Era
(roughly 600 million years ago) allowed animals to
become large and leave fossils. How important was
oxygen for the process of early animal evolution? New
data show that some modern sponges can survive for
several weeks at low oxygen levels. Many groups of
animals have mechanisms to cope with low oxygen or
anoxia, and very often, mitochondria organelles usually
associated with oxygen are involved in anaerobic
energy metabolism in animals. It is a good time to refresh
our memory about the anaerobic capacities of mitochondria in modern animals and how that might relate to
the ecology of early metazoans.
.
Keywords:
anaerobiosis; eukaryotes; geochemistry; hypoxia;
mitochondria; Neoproterozoic ocean chemistry;
rhodoquinone
Introduction
Humans are oxygen guzzlers. An adult human consumes
about 700 L of molecular oxygen (O2) per day [1], the vast
majority of which serves ATP synthesis in our mitochondria,
where about a bodyweight of ATP is produced each day to run
our bodies and keep our species (and its evolution) going. If
we look around at other large animals that live on land, they
are all specialized to life with O2 in the atmosphere, which
should not be too surprising, because vertebrate life on land
only goes back about 350 million years (My) [2], and arose at a
time when there was roughly as much (or more) oxygen in the
atmosphere as there is now: about 21% by volume [3]. But
there was not always oxygen to breathe. Though O2 started
accumulating in the atmosphere about 2.4 billion years (Gy)
ago, its accumulation in the oceans was a much slower
process, and many lines of evidence indicate that the
oxygenation of the oceans came to completion less than ca.
600 My ago [3, 4], close to the time when the first animals
appear in the fossil record [5].
The appearance of the first fossil animals 580 My ago [6],
or even earlier [7], and the appearance of the first fossil
sponges 535 My ago [8] does not mean that those groups
arose at that time. Molecular data have it that metazoan
radiation pre-dated the appearance of the first fossil animals
DOI 10.1002/bies.201400060
1)
2)
3)
4)
5)
Faculty of Natural Sciences, Department of Biochemistry, Comenius
University, Bratislava, Slovakia
Institute of Molecular Evolution, University of Düsseldorf, Düsseldorf,
Germany
Department of Biological Sciences, University of Alberta, Edmonton, AB,
Canada
Faculty of Veterinary Medicine, Department of Biochemistry and Cell
Biology, Utrecht University, Utrecht, The Netherlands
Department of Medical Microbiology and Infectious Diseases, Erasmus
University Medical Center, Rotterdam, The Netherlands
Abbreviations:
AFDW, ash-free dry weight; DW, dry weight; FRD, fumarate reductase; gDW,
gram dry weight; GOE, great oxidation event; Gy, billion years; HMA, highmicrobial abundance sponge; LECA, last eukaryotic common ancestor; LMA,
low-microbial abundance sponge; My, million years; NOE, neoproterozoic
oxidation event; OMO, organelles of mitochondrial origin; PAL, present
atmospheric levels; RQ, rhodoquinone; SLP, substrate level phosphorylation;
WW, wet weight.
*Corresponding author:
William F. Martin
E-mail: [email protected]
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Has a modern sponge preserved
ancestral states?
Though we cannot turn back time, we can look at
representatives from early branching lineages in the hope
that they have preserved some primitive traits. This is the
approach that Mills et al. [10] recently undertook. They
collected samples of the aerobic marine invertebrate Halichondria panicea (a sponge) from well-oxygenated surface
waters of Kerteminde Fjord in Denmark and tested their
respiration rate, feeding rate, and overall well-being under a
wide range of oxygen concentrations. They showed that
H. panicea is able to respire, feed, and grow under a lowoxygen gas phase corresponding to 0.54% present atmospheric levels (PAL). The animals remained healthy for
24 days, and the experiment was terminated before the
animals completed their life cycle. From this comparatively
simple observation combined with the presumption that such
“levels may have been present in the environment well before
animals originated”, they infer that “animal evolution may not
have been prohibited by the presumably low atmospheric
oxygen levels before the Neoproterozoic Era.” The strength of
that conclusion hinges upon the assumption that H. panicea
has preserved the ancestral condition with regard to oxygen
requirements, as any modern taxon might exhibit uniquely
derived or shared derived features that set it apart from its
ancestors.
Taxonomically, H. panicea belongs to the demosponges,
one of four classes of the phylum Porifera [11]. Sponges
traditionally occupy earliest branches on phylogenetic trees of
all animals [12]; according to some studies they are the sister
group to all other known animal species [13]. Their anatomy is
unique: They have flagellated feeding cells called choanocytes
facing internal chambers, and canals through which water
flows, supplying the organism with microscopic food-such as
the cryptophyta alga Rhodomonas sp. used in the study for the
purpose of feeding H. panicea [10]. Choanocytes morphologically resemble choanoflagellates, single-celled eukaryotes
that are the closest living relatives of all animals [14]. Relying
on phylogenetic trees showing Porifera as the earliest
diverging animal lineage, Mills et al. [10] surmise that modern
demosponges serve as analogs for early animals, and that
“because the last common ancestor of all living animals likely
had a sponge-like body plan, the physiology and oxygen
requirements of modern sponges should serve as a reasonable
window into the oxygen requirements of the earliest animals.”
Based on that, and given the observed tolerance of H. panicea
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to low oxygen levels, they conclude that the oxygen demands
of the last common ancestor of metazoans “may have been met
well before the enhanced oxygenation of the Ediacaran Period.
Therefore, the origin of animals may not have been triggered
by a contemporaneous rise in the oxygen content of the
atmosphere and oceans.”
Notwithstanding some ambiguity with regard to the word
“origin” (phylogenetic origin of the lineages? or their
appearance in the fossil record?), one might agree with their
conclusion, but there are some caveats en route to getting
there. There are an estimated >14,000 species of sponges [11],
and it would have been good to see results from representatives from some of the other groups. The observed oxygen
requirements of modern demosponges are one thing, but the
conclusion that this reflects the unaltered ancestral state of
sponge (or animal) physiology carries with it the assumption
that nothing has changed during the 700 million years of
evolution in the lineage leading to the sponge that they
studied. Geochemists currently paint a picture of profoundly
changing environmental conditions especially at the late
Proterozoic/Phanerozoic Eons boundary [3, 15] such that the
habitat of the earliest animals, probably shallow ocean, was
fluctuating from hypoxic and very often anoxic and euxinic at
biologically productive ocean margins to well oxygenated
even at deeper depths [3]. The environments inhabited by the
first demosponges, the environments inhabited by the earliest
animals that left fossil traces, and the environments inhabited
by the earliest animals are not necessarily all the same
regarding their redox structure and oxygen availability [3].
And what if sponges do not represent the body plan (or the
physiology) of the last common ancestor of all living animals?
Not all phylogenetic studies place sponges as the sister lineage
to all other animals [12]. Recent phylogenies accompanying
the genome sequences of the ctenophores Mnemiopsis
leidyi [16] and Pleurobrachia [17] indicated that ctenophores
(comb jellies) might be basal to all animals, including
sponges. Accordingly, the nature of the metazoan common
ancestor remains debated [18]. Another caveat is lineage
sampling. While Mills et al. [10] looked at one species,
H. panicea, recent transcriptomic investigations of eight
species from all four classes of the phylum Porifera uncover
unexpected genetic complexity among the sponges [19] and
support the view that some sponges might have lost some
ancestral cell types, and possibly physiological processes,
along their evolutionary route.
Clearly, the experiments reported by Mills et al. [10] do
show that H. panicea demosponge species can survive harsh
hypoxic conditions (34% PAL) for relatively long periods:
24 days in their study. But it has long been known that many
invertebrates, and even some vertebrates, can survive longer
periods with even less oxygen [2022]. The goldfish Carassius
auratus can survive complete anoxia for more than a week at
10˚C [23] and the carp Carassius carassius can withstand
anaerobiosis for months (140 days) at 2˚C [24]. These fish
maintain their vitality through ethanol fermentation, excreting the end products of their anaerobic metabolism, ethanol
and CO2, into the surrounding water. There are several
pathways leading to ethanol fermentation in eukaryotes, but
in the cases known so far they are cytosolic pathways [25], so
the carp mitochondria apparently do not participate in energy
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by many millions of years [9]. The implication is that the first
animal groups, which evolved from unicellular eukaryotes
(protists), arose at a time before the oceans were fully oxic.
This makes information about the ecology and habitat of the
first animals all the more interesting. Knowing the oxygen
requirements of the earliest animals would provide insights
into the nature of the energy metabolism of our primitive
metazoan predecessors. At the same time, it would shed light
on the environmental conditions to which early animals were
adapted.
M. Mentel et al.
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M. Mentel et al.
Prospects & Overviews
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What was the ancestral state of animal
energy metabolism?
metabolism under those conditions. It is not known which
metabolic end products H. panicea generated during the 24day incubation, or whether their mitochondria were involved.
Mills et al. [10] measured oxygen consumption, but it is hard to
tell from the data available how much of that might have been
performed by bacterial symbionts, and many eukaryotic
organisms with an anaerobic energy metabolism nevertheless
have oxygen consuming pathways in the cytosol that are
distinct from mitochondrial respiration.
It is difficult to compare Mills et al.’s [10] respiration data
with work on other sponges including data from the same
species carried out previously [26] because of the different
units of measurement used. But clearance rates reported by
Mills et al. [10] of 800 algal cells/mL hour are 40% of those
found in previous work (2,0004,000 cells/mL hour) [26, 27];
and respiration rates, if reported per gram dry weight (gDW)
of sponge tissue (as in Table 1), are 30% of those reported
earlier (10 mM/L hour gDW, compared with 26.8 mM/L hour
gDW) [26]. Reduced filtration comes with reduced energy
intake. At 1.75 mJ/cell [28] 800 algal cells would provide the
sponge with 1.4 J/hour, but a respiration rate of 10 mM/L hour
gDW means that 4.3 J/hour are required for metabolism.
Considering that the sponge in Mills et al. [10] experiment
filtered (a cost for other sponges of about 16% of available
oxygen) and even grew branches, there is a deficit. This could
have been made up by filtration of bacteria (which were not
counted here). It is also possible that other factors, such as
anaerobic energy metabolism, might have been involved.
Transcriptomic data from the sponge they cultured would
have shed some light on which biochemical routes it was
employing, because the roughly 50 enzymes involved in
anaerobic energy metabolism among eukaryotic groups are
reasonably well characterized [25].
In our view, the reconstruction of oxygen requirements and
metabolic traits of the earliest animals and ancestral
metazoans is best understood in the context of energy
metabolism of eukaryotes, of which the animals are just one
lineage in general. Most scientists would agree that eukaryotes originated at least 1.5 Gy ago, as fossils clearly
representing eukaryotic protists are found in rocks of that
age [29, 30], and molecular estimates for the timing of
eukaryotic evolution are consistent with that view [8, 31, 32].
Thus, eukaryotes can be taken to have arisen about 1.6 Gy ago,
at a time when anoxic environments were more widespread
than at the dawn of animal evolution, almost a billion years
later. What were the oxygen demands of the first eukaryotes?
Currently, there are two mutually exclusive views about
oxygen demands of early eukaryotes and their subsequent
evolution.
One view has it that the earliest eukaryotes were strict
aerobes, which at different occasions and by means of interdomain and intradomain horizontal (lateral) gene transfer adapted to hypoxic and anoxic conditions [3335]. Proponents of this view argue that early eukaryotes were unable to
survive hypoxia, but instead had to acquire genes via lateral
transfer in order to gain ecological access to anaerobic
environments [3439].
We favor the alternative view that the free-living ancestors
of mitochondria were themselves facultative anaerobes with a
diversity of bioenergetic enzymes [40], and that the earliest
eukaryotes possessed facultatively anaerobic mitochondria [25]. This allowed them to extract energy from their
environment and survive under a wide range of environmental
Table 1. Respiration and filtration rates of sponges
Respiration rate
Per ml of sponge
Species
Neogombata magnificaa
Theonella swinhoei
Mycale sp.b
Tethya cryptac
Verongia gigantead
Verongia fistularise
Halichondria panicea
Halichondria panicea
(mmol O2/hour)
2.22
1.38
1.965
0.893
3.036
4.736
1.936
Filtration rate
Per gDW
Removal efficiency
Per ml of sponge
(%)
(L/hour)
0.63
0.156
0.756
0.158
0.191
0.44
0.12h
0.048i
(mM)
14.88
46.58
7.42
31.34
33.58
26.8f
7.93f
1013g
42
1.2
1.1
5.6
5.3
9
2.23
1.78
10.72
10.6
Per gDW
4.2
10.75
1.31
1.908
3.12
1.7
0.68i
Refs.
[78]
[79]
[80]
[80]
[80]
[81]
[26]
[10]
One milliliter sponge volume ¼ 1 g wet weight (WW); DW ¼ 15% WW; AFDW ¼ 12% WW.
One milliliter sponge volume ¼70 mg DW; AFDW ¼ 70.3% DW.
c
One milliliter sponge volume ¼ 100 mg; AFDW ¼ 65% DW.
d
One milliliter sponge volume ¼ 121 mg; AFDW ¼ 37.8% DW.
e
One milliliter sponge volume ¼ 1.2 g WW ¼ 0.141 g DW ¼ 0.103 g AFDW.
f
Saturated oxygen.
g
Reduced oxygen (11, 4, and 3% PAL ¼ 27.5, 10, 7.5 mM).
h
Reflecting clearance of 2,000 Rhodomonas cells/L hour.
i
Ratio of reported clearance of 800 Rhodomonas cells/L hour to rate reported by Thomassen and Riisgård [26].
a
b
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Figure 1. Schematic phylogeny of protists and animals harboring anaerobic mitochondria, hydrogenosomes, or mitosomes, schematically
indicating the higher order phylogeny of eukaryotes that groups all known eukaryotic diversity into six major clades called “supergroups” [9,
74]. Internal branching order within the clade of animals is based on Dunn et al. [12]. Note that regardless of whether the position of the root
of the tree is as shown, or is basal to opisthokonts [8, 74], or is on the excavate branch as new findings suggest [75], the distribution of
organelles of mitochondrial origin with anaerobic capabilities spans groups on either side of the root. Also note that the many lineages with
aerobic mitochondria (occurring in all supergroups) are not shown in the figure. Organelle classification as in Müller et al. [25]. The nature of
energy metabolism of sponge mitochondria (bold) is uncertain, highlighted by the question mark. Encircled “DNA” indicates the presence of a
genome in the respective mitochondrial type. LECA, last eukaryotic common ancestor.
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Figure 2. Generalized metabolic scheme of major pathways in anaerobic mitochondria
(class 2). Inside the mitochondrion malate dismutation resulting in the production of
acetate, succinate, and propionate is shown together with the corresponding anaerobic
electron-transfer chain, while for comparison the Krebs cycle and corresponding aerobic
electron-transfer chain are shown in gray. The propionyl-CoA cycle that is used to
convert succinate to propionate is simplified and shown as a linear pathway (see [25] for
details). Modified after [25, 55, 63]. For other examples of anaerobic energy metabolism
in animal mitochondria, see [20, 23]. CI to CIV, respiratory complexes I to IV; UQ,
ubiquinone; RQ, rhodoquinone; C, cytochrome c; A, ATPase; FRD, fumarate reductase;
1, phosphoenolpyruvate carboxykinase (ATP dependent); 2, malate dehydrogenase; 3,
malic enzyme; 4, pyruvate dehydrogenase complex; 5, acetate:succinate CoA-transferase; 6, succinyl-CoA synthetase; 7, fumarase. Note that the NADH-dependent fumarate
reductase of protists and the quinone-dependent fumarate reductase of animal
mitochondria are different enzymes (see [25] for a discussion).
conditions, including different concentrations of oxygen and
sulfide [25, 41, 42]. Under this view, the ability of eukaryotes
to survive in anaerobic environments was present in the
eukaryote common ancestor. This would directly account for
the findings that (i) anaerobes are interspersed all across the
tree of eukaryotic life, interleaving with their aerobic relatives,
and (ii) that to survive hypoxic and anoxic conditions,
different eukaryotes use overlapping subsets of a set of about
50 enzymes that were present in the eukaryote common
ancestor [25]. Because enzymes for aerobic and anaerobic
energy metabolism were present in the eukaryote common
ancestor, their vertical inheritance into the common ancestor
of animals is not surprising, nor is the differential loss of
unneeded enzymes in lineages that have specialized to
strictly aerobic and anaerobic habitats, respectively. In animal
928
lineages that are regularly confronted with
anoxia, the enzymes have been preserved in
cases studied so far [25].
How do eukaryote
anaerobes do it?
When the endosymbiotic theory for the
origin of organelles was being revived in the
1970s, oxygen was seen as the factor that
triggered the origin of mitochondria [43]. At
that same time, hydrogenosomes were
being discovered [44], which turned out
to be anaerobic forms of mitochondria from eukaryotes that
inhabit anoxic environments [45]. Today we know five
different functional classes of mitochondria, all descended
from one and the same endosymbiotic event [25]: classical
aerobic mitochondria (class 1) such as those found in rat liver;
anaerobic mitochondria (class 2) as are found among several
groups of invertebrates [46, 47]; hydrogen-producing mitochondria (class 3), which have so far only been found in
ciliates, but might also be present in Blastocystis [4851];
hydrogenosomes (class 4), which occur in anaerobic groups
of fungi, ciliates, trichomonads, and other protists; and
mitosomes (class 5), which are being found in an increasing
number of eukaryotic groups [45, 52]. Of the five classes of
organelles of mitochondrial origin (OMOs), all but class 5
generate ATP from the breakdown of carbon compounds, but
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Figure 3. Distribution of genes
for anaerobic energy metabolism
in sponges and eukaryotes. The
right portion of the figure is for
reference and is slightly modified
from Müller et al. [25]. The left
portion of the figure was prepared
as described in [25] by BLASTing [76] the query sequences
against sponge EST data from
Riesgo et al. [19], downloaded
from http://thedata.harvard.edu/
dvn/dv/spotranscriptomes. To
check for bacterial or protistan
sequences, the sponge ESTs
meeting the criteria for inclusion
in the figure (Blast e-value of
1010 and >25% local amino
acid identity) were reblasted to
GenBank; sequences from the
sponge EST data hitting prokaryotes only were scored as absent
(a list of the sequences so scored
is listed in Supplementary
Table S1). Note that two forms of
fumarate reductase exist in eukaryotic anaerobes: the soluble
NADH-dependent enzyme, for example from Trypanosoma [25],
and the membrane bound rhodoquinone-utilizing enzyme, for example from from Ascaris
mitochondria [77].
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M. Mentel et al.
only class 1 and dependent on environmental conditions
or life cycle stage class 2 generate ATP with the help of
molecular oxygen [25]. As far as is known now, only class 1
and 2 mitochondria are present in the animal lineages.
Anaerobic forms of mitochondria occur in all of the six
major groups of eukaryotes that biologists currently recognize.
That traces the ability to survive in anaerobic environments to
the eukaryote common ancestor (Fig. 1), hence its persistence
in the animal lineage should hardly be surprising. Moreover,
the enzymatic machinery that is used in the anaerobic
mitochondria of different animal groups represents variations
on a common theme. The typical end products of energy
metabolism in metazoan anaerobic mitochondria are CO2,
acetate, succinate, and propionate [21, 25, 53, 54]. Among the
animal lineages, the enzymatic details of anaerobic mitochondria have been studied only in a few model organisms [25].
The model systems reveal, however, minor variations on a
conserved common theme called malate dismutation [55].
During malate dismutation in anaerobic mitochondria
(Fig. 2), malate and not pyruvate is the end product of
cytosolic glucose degradation. A portion of the imported
malate is oxidized first to pyruvate and then to acetyl-CoA; in
both reactions NADH is produced, which donates electrons to
complex I. Acetyl-CoA is the substrate for a CoA transferase
that generates succinyl-CoA, which produces one ATP via
substrate level phosphorylation (SLP), and acetate as an
excreted metabolic end product. Another portion of the malate
is converted to fumarate by a Krebs cycle reaction running
backwards, and fumarate serves as the terminal acceptor for
the electrons transferred to complex I by the NADH produced
during acetate production. Fumarate is reduced by fumarate
reductase (FRD), generating succinate, which many animals
excrete as an end product. In other animals with anaerobic
mitochondria, the succinate is further converted to propionate, generating an additional ATP via SLP. When operating in
redox balance, two propionate molecules are generated for
every acetate, because two malate molecules have to be
reduced in order to reoxidize the two NADH generated during
the synthesis of one acetate. Acetate plus propionate
production via malate dismutation generates approximately
five ATPs per glucose: 2 mol ATP per glucose in the cytosol,
and inside the mitochondria 1 mol ATP for each acetate and
propionate produced. In addition, ATP is formed via proton
pumping at complex I and the mitochondrial ATP synthase
(1 ATP per glucose), but without the use of oxygen.
The flow of electrons from NADH at complex I to fumarate
at FRD in malate dismutation requires a special quinone
with a midpoint potential lower than that of ubiquinone.
Accordingly, metazoan anaerobic mitochondria use rhodoquinone (RQ) instead. RQ has a fairly restricted distribution in
nature. It is found in facultatively anaerobic alpha-proteobacteria, such as Rhodobacter [56], where it was first described, a
few other isolated proteobacteria, and in eukaryotes with
anaerobic mitochondria. RQ is best studied in the anaerobic
mitochondria of metazoan parasites such as the liver fluke
Fasciola hepatica [57] and Ascaris suum, an intestinal
worm [58], but it also occurs in free-living metazoans such
as Caenorhabditis elegans [59], and in protists such as
Euglena [60]. The biosynthesis of RQ has still not been fully
resolved, either in prokaryotes or in eukaryotes, but it is a
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rather specific biochemical trait that could link the origin
of mitochondria to facultatively anaerobic bacteria. Anaerobic
mitochondria in animals, and the ability of some animal
mitochondria to tolerate high sulfide concentrations and
even to use electrons from H2S for ATP synthesis [61], are
readily seen as holdovers from the early days of animal
evolution [41, 62]. That animals have preserved many
biochemical relicts from their not-so-distant anaerobic past
is not a new idea [41, 42, 46], but it fits nicely with the new
report on sponge growth, even though we do not yet know
what the sponge mitochondria in the specimen that Mills
et al. [10] investigated are doing.
Even though no EST data were reported for H. panicea, we
looked for the presence of transcripts for genes of anaerobic
energy metabolism in the EST data recently published by
Riesgo et al. [19] for representatives from several sponge
lineages. Although the sponges in that study were not grown
under low oxygen conditions, both animals and protists with
anaerobically functioning mitochondria tend to be prepared
for anaerobiosis before its onset. That is, the enzymes for
anaerobic energy metabolism are present before anoxia is
encountered [60, 63, 64]. The sponge EST data of Riesgo
et al. [19] harbor no surprises: the enzymes for anaerobic
energy metabolism known from other animals with anaerobic
abilities are present (Fig. 3). Of particular interest are
transcripts for the enzyme sulfide:quinone oxidoreductase,
which deals with H2S in animal mitochondria [41, 65, 66].
More than mitochondria
The story of oxygen is not only about mitochondria: collagen
and sterols are two cases in point. Metazoans typically use
collagen as their structural support [67], and collagen requires
molecular oxygen for its synthesis because of its many
hydroxyproline residues [68]. Thus, one view has it that
animals did not originate as an evolutionary lineage with the
rise of oxygen during the neoproterozoic oxidation event
(NOE): rather they were already there and just became bigger
because there is a correlation between oxygen levels and
body size [69] and collagen made their bodies rigid enough
to start leaving fossils [70]. That would be consistent with
phylogenetic data that has the origin of animal lineages well
predating their appearance in the fossil record [9].
To be sure, we are not suggesting that rising marine
oxygen levels 580 My ago exerted pressure on early animal
lineages to evolve into bigger and more easily fossilized forms.
Increased oxygen levels merely created permissive conditions,
allowing those animals to arise that acquired the corresponding mutations. A similar situation is found in the Carboniferous, where atmospheric oxygen levels were very high (up to
150% PAL) and permitted many preexisting insect lineages,
including the giant dragonflies, to become much larger [71].
The matter of oxygen and sterol synthesis is related to
the role of oxygen at the eukaryote origin rather than at the
animal origin, but also comes into play. The eukaryote sterol
synthesis pathway does require molecular oxygen, but how
much oxygen? Waldbauer et al. [72] recently found that for
sterol biosynthesis, yeast requires only trace amounts of O2,
corresponding to 7 nM in solution. For comparison, current
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Conclusion
And what are the sponge mitochondria in the report by Mills
et al. [10] doing? No end products or gene expression data
were reported, so we can only guess, and it is possible that the
mitochondria were doing nothing cytosolic fermentations
might have been involved, and it is not clear how much of the
oxygen consumption they measured was attributable to
bacteria associated with the sponge, rather than the sponge
itself. Indeed, another strategy that animals use to survive
hypoxia is metabolic arrest: the animal simply brings
metabolism close to a halt and waits for better times [73].
Whatever future studies of the anaerobic metabolism of
sponges reveal, it seems likely that we will not see a
fundamentally new form of anaerobic animal energy
metabolism, rather just more variations on a theme that
was present in the common ancestor of animals. Whether
sponges are indeed the first animals is a phylogenetic
question. Whether they have preserved ancestral metabolic
traits is a biochemical issue that hinges on knowledge about
the specifics of energy metabolism in their mitochondria.
The mitochondria of diverse invertebrate lineages can respire
oxygen at presently available levels and can perform malate
dismutation under anaerobic conditions [25, 46]. This clearly
suggests that the first animals could do the same and thus
possessed facultatively anaerobic mitochondria with fumarate
reductase and RQ. Hence, the ability of sponges to survive
low oxygen does not come as a surprise, and knowing what
sponge mitochondria do under anaerobic conditions will
improve our understanding of energy metabolism in an earlybranching animal lineage.
The authors have declared no conflict of interest.
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