NEWS & VIEWS doi:10.

1038/nature23539

BIOG EO CHEMISTRY years after the photosynthetic capacity of algae

had evolved? And what does this have to do

Food for early with animal evolution? This is where ecological

theory fits in.
In modern oceans, picoplankton (those

animal evolution
up to 2micrometres in diameter), especially
the photosynthetic cyanobacteria, dominate
primary production in low-nutrient environ-
ments that occur in certain mid-ocean loca-
A revised timeline for when algae became ecologically important among plankton tions6. Experiments and modelling support
in the ancient oceans reveals a link between chemical changes in those waters and the idea that, as nutrient availability increases,
the emergence of animals in marine ecosystems. picoplankton populations expand7. How-
ever, their ready availability as a food source
can then limit the picoplankton population
ANDREW H. KNOLL were sparse and potentially compromised because they are eaten by other organisms,
by sample contamination. providing an opportunity for larger primary

E
ver since microorganisms first emerged,
Earth and the life upon it have engaged
in something of a pas de deux. Seldom
during this long history have the dances
tempo and the dramatic heights of the jet
leaps exceeded those that occurred near the
end of the Proterozoic eon, which spanned the
time from 2.5billion to 541million years ago.
A supercontinent broke apart and then began
to reassemble; ice ages twice whitened the
planet from pole to Equator; and redox condi-
tions underwent a fundamental shift. Amid all
of this, animals large enough to be visible to
the eye arrived on the scene, among them the
bilaterians, which are symmetrical along their
front-to-back axis, have complex organs and
overwhelmingly represent present-day animal
diversity.
Scientists have long viewed these develop-
ments as being intertwined, but the timing of
key events and the mechanisms of interaction
remain contentious. Resolving these debated
points will require geologists to precisely
date events documented in the rock record,
and biologists to articulate mechanisms that
illuminate the relationship between life and
the surrounding physical environment. In a
paper online in Nature, Brocks etal.1 make a
substantial contribution to both, reorienting
discussions of early animal evolution.
Brocks and colleagues focused initially on
primary producers organisms that fix car-
bon dioxide into sugar, generating the organic
compounds needed to sustain life throughout
ecosystems. The authors meticulously ana-
lysed a large collection of organic-carbon-rich
sedimentary rocks from the Neoproterozoic
era (from 1billion to 541million years ago).
Lipids extracted from these rocks provide sig-
natures of both bacteria and algae, and record
the changing composition of photosynthetic
plankton in ancient marine ecosystems2.
Previous studies2 demonstrated that green
algae were the key primary producers in the
oceans by the Ediacaran period (635million to
541million years ago), but data for earlier times
The authors reveal that lipids produced producers to grow instead7. Thus, Brocks and
by algae first occur in rocks that are dated colleagues observation of the Neoprotero-
between two global ice ages from the end of zoic expansion of nanoplanktonic green algae
the Sturtian ice age, approximately 663million (those of 220micrometres in diameter) prob-
years ago3, to the beginning of the Marinoan ably reflected an increase in nutrient levels in
ice age, 645million years ago (Fig.1). Reassur- the oceans of that time.
ingly, the authors proposed time frame for the Analyses of phosphate abundances in sedi-
rise of planktonic algae is consistent with esti- mentary rocks suggest a fundamental change
mates made using molecular clock analyses in phosphate availability during the Sturtian
of genetic differences between modern marine ice age8, at a time just before the algal-lipid
plankton4. The timing also fits with a late- increase observed by the authors. Molecular-
Neoproterozoic change in the carbon-isotope clock analysis also suggests that nitrogen-
composition of sedimentary-rock-associated fixing cyanobacteria prominent in modern
lipids that is interpreted as a shift from bacte- oceans have late-Neoproterozoic origins9, per-
rial to algal sources of organic matter buried haps documenting a nitrogen-cycle response
in sediments5. to the increase in phosphate fluxes. Ecological
The time window of the algal rise to ecologi- models10 predict that, as a shift towards larger
cal prominence now seems secure. But what primary producers occurs, more energy and
drove the rise of algae in productive ocean carbon should become available to organisms
waters at this time, hundreds of millions of higher in the food chain, thereby providing a
Ecosystems in transition
Low oxygen High oxygen
Cyanobacteria are the Algae become ecologically Animal
dominant plankton important plankton diversification
Marine phosphate
levels begin to increase
Sturtian ice age Marinoan ice age
Tonian Cryogenian Ediacaran
750 700 650 600 550 541
Millions years ago
Figure 1 | The rise of algae. Brocks et al.1 extracted and analysed lipids from marine rocks from the
Neoproterozoic era (1billion to 541 million years ago), enabling them to refine the proposed time
frame for when algae became ecologically important photosynthetic plankton. This insight allows the
rise of algae to be better understood in the broader context of other biological and physical changes
that occurred on Earth around that time, particularly when ecosystems were in transition during the
Cryogenian and Ediacaran periods, a time when oxygen levels were increasing in the atmosphere and
oceans. The authors propose that an increase in marine phosphate levels facilitated the rise of algae.
Algae might have provided early animals with a food source that aided their survival and diversification.

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 RESEARCH NEWS & VIEWS

resource boost for early animals. Thus, food-
source changes might have helped to pave the
way for Ediacaran animal radiation.
Brocks et al. propose that intense weather-
ing that immediately followed the Sturtian
glaciation was the source of increased marine
phosphate levels that would have facilitated
planktonic algal radiation. However, because
sedimentary phosphate abundances changed
during the Sturtian ice age, an earlier time in
the record should be examined for insight into
phosphate enhancement, using an approach
that focuses less on transient events and more
on factors that govern long-term states of
Earths physical environment.
One possibility is that oxygen has regulated
phosphate availability through time11. At low
oxygen levels a state thought to character-
ize the Proterozoic Earth12 iron oxidation
might have trapped much of the phosphate
released by weathering of rocks through phos-
phate adsorption on mineral surfaces before it
could reach the oceans11. An increase in oxy-
gen levels would cause this phosphate trap to
disappear, resulting in a substantially increased
phosphate flux into the oceans. At the same
time, the low-oxygen and iron-rich waters of
Proterozoic oceans constituted major sinks
for seawater phosphate that would have been
attenuated when oxygen levels increased13.
Some models11 predict that an increase in
oxygen during global glaciation causes a self-
sustaining state change in nutrient availabil-
ity. Once such a system is set in motion, the
oxygenation of subsurface ocean water masses
should reduce mineralogical phosphate sinks,
and the resulting higher levels of primary
production should increase the rates of
organic-carbon burial on the ocean floor. This,
in turn, would facilitate an increase in oxygen
production, ushering in a new biosphere redox
state by the late Ediacaran.
Thus, oxygen, long recognized as a meta-
bolic gatekeeper for animal evolution, might
also have mediated the availability of nutrients
in ancient marine ecosystems. An increase in
food availability, an enhancement in the trans-
fer of energy upward through food chains,
and a decline in hazardous low-oxygen waters
might all have complemented the metabolic
opportunities that increasing oxygen levels
provided for early animals. Of course, there
may be other ways to thread the needle.
Models reflect what we know, and future dis-
coveries might result in changes to both our
understanding of age relationships between
geologically observed events and how much
we emphasize specific processes.
Key questions about the history of oxygen
levels remain. The view that Proterozoic eco-
systems had more oxygen than their earlier
Archaean counterparts (of more than 2.5bil-
lion years ago) but less than those of modern
times is reasonable, but a more quantitative
understanding of this history remains elu-
sive. Better models than those currently
available are needed to describe phosphate
and nitrogen cycling in the Proterozoic bio-
sphere, and an improved understanding of the
physiological characteristics of early animals
is also required14,15. Brocks and colleagues
contribution will change the conversation.
Continuing discussions of early animal
evolution can now be embedded in a more-
complete ecosystem framework that includes
primary producers.
Andrew H. Knoll is in the Department
of Organismic and Evolutionary Biology,
Harvard University, Cambridge,
Massachusetts 02138, USA.
e-mail: aknoll@oeb.harvard.edu
1. Brocks, J. J. et al. Nature http://dx.doi.org/10.1038/
nature23457 (2017).
2. Knoll, A. H., Summons, R. E., Waldbauer, J. R. &
Zumberge, J. E. in Evolution of Primary Producers in
the Sea (eds Falkowski, P. & Knoll, A. H.) 133163
(Elsevier, 2007).
3. Rooney, A. D. et al. Proc. Natl Acad. Sci. USA 111,
5156 (2014).
4. Snchez-Baracaldo, P., Raven, J. A., Pisani, D. &
Knoll, A. H. Proc. Natl Acad. Sci. USA http://dx.doi.
org/10.1073/pnas.1620089114 (2017).
5. Close, H. G., Bovee, R. & Pearson, A. Geobiology 9,
250265 (2011).
6. Chisholm, S. W. in Primary Productivity and
Biogeochemical Cycles in the Sea (eds Falkowski, P.G.
& Woodhead, A. D.) 213237 (Plenum, 1992).
7. Ward, B. A., Dutkiewicz, S. & Follows, M. J.
J.Plankton Res. 36, 3147 (2014).
8. Reinhard, C. T. et al. Nature 541, 386389 (2017).
9. Snchez-Baracaldo, P., Ridgwell, A. & Raven, J. A.
Curr. Biol. 24, 652657 (2014).
10. Knoll, A. H. & Follows, M. J. Proc. R. Soc. B 283,
20161755 (2016).
11. Laakso, T. A. & Schrag, D. P. Geobiology 15,
366384 (2017).
12. Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. Nature
506, 307315 (2014).
13. Derry, L. A. Geophys. Res. Lett. 42, 85388546
(2015).
14. Sperling, E. A., Knoll, A. H. & Girguis, P. R. Annu. Rev.
Ecol. Evol. Syst. 46, 215235 (2015).
15. Hoyal Cuthill, J. F. & Conway Morris, S. Nature Ecol.
Evol. 1, 12011204 (2017).

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