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Geobiology (2003), 1, 3 14

The geological consequences of evolution


O RIGINA
Blackwell
Geological L A R T I CLtd.
Publishing L E of evolution
consequences

A ND R E W H . K N O L L

Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

ABSTRACT

Geobiologists seek to understand the role of organisms in the Earth system. By extension, one can ask how
evolutionary innovations and, more generally, the population genetic processes that mediate evolution have
influenced the Earths surface through time. The example of oxygenic photosynthesis and the redox history of
atmospheres and oceans illustrates the complex relationship between evolution and environmental change.
Biological innovations determine the dimensions of biological participation in the Earth system, but by them-
selves they seldom generate lasting environmental change. More commonly, environments change when
physical drivers exceed the limited environmental buffering capacity conferred by population genetics and
nutritional codependence. Environmental change, in turn, feeds back on biology, creating new opportunities for
evolutionary innovation.

Received 05 December 2002; accepted 05 February 2003

Corresponding author: Professor Andrew H. Knoll. Tel.: 001 617 495 9306; e-mail: aknoll@oeb.harvard.edu

which the consolidation and uplift of marine sediments (driven,


INTRODUCTION
in his view, by heat) completed a cycle that linked erosion and
Geobiology is widely appreciated as a new enterprise within deposition. Habitats for plants and animals were maintained
the Earth sciences. It may therefore come as a surprise that the dynamically by what Hutton (1785) called the System of
founding document of geobiological thought is none other the Earth.
than the foundational text of modern geology, James Huttons Interestingly, despite Huttons biological motivation, life
(1788) Theory of the Earth. Much as Charles Darwin (1859) contributes little in the way of process to the dynamics of his
did in The Origin of Species, Hutton carefully documented Earth system. As Lovelock (1989) has observed, Hutton did
what he saw around him commonly, quotidian observations liken the Earth to a superorganism, but taken in context, this
that anyone might have made. But, again like Darwin, Hutton has to be understood as metaphor, not archae-cybernetics
marshalled his observations in support of a sophisticated Huttons imagery did not imply that biological physiology
and, in its time, revolutionary worldview. Huttons arguments contributed substantially to geophysiology. There is passing
strike the 21st century reader as surprisingly modern, but then acknowledgement that plants may speed erosion by contribut-
our sense of modernity in geological thought derives in no ing to the breakup of rocks, but in general life is simply served
small measure from Hutton himself. by a physical system.
Hutton explicitly asked how the Earth can maintain itself The idea that life itself constitutes a suite of geologically
as a habitable planet. In true late eighteenth century fashion, important processes is much more recent, surfacing early in
he observed that the distribution of land and sea provides the last century in the writings of Vernadsky (1926) and, more
habitats well suited for plants and animals. Hutton also noted, recently (and famously), in James Lovelocks (1979) concep-
however, that erosion inexorably if slowly wears down the tion of Gaia. Of course, Gaia itself sometimes seems to be
land, while sediments supplied by rivers continually fill in the suspended uncomfortably between metaphor and systems
sea. How then can the Earth continue in the long term as an science. As research focuses ever more resolutely and with
abode for life? increasing maturity on the Earth system, it is useful to ask what
Hutton recognized that sustained habitability cannot roles are played by the systems constituent parts, and how
depend on environmental stasis, because the land and sea are changes in individual parts may influence the system as a whole.
demonstrably not static. One further observation, however, That is the nature of the question I wish to explore in this
suggested an alternative explanation. Sedimentary rocks in the essay. I will not consider in detail whether or how biological
hills and mountains of Scotland contain the fossilized shells of processes contribute to the maintenance of the Earth system
marine animals, prompting Hutton to conceive of a world in it is well understood that they do, and many scientists have

2003 Blackwell Publishing Ltd 3


4 ANDREW H. KNOLL

contributed to the elucidation of the mechanisms by which parent (bacterio)chlorophyll and gets passed in bucket brigade
this occurs. Rather, I wish to ask a subtly different question: fashion through a chain of redox reactions, eventually to drive
How and to what extent have processes of evolution contrib- formation of reducing power in the form of NADPH and
uted to the changing state of Earth surface environments? The chemical energy, as ATP. The electron transport chain can be
fact that biology participates significantly in the Earth system cyclic that is, the electron, stripped of its energy, can be
does not necessarily mean that biological evolution drives returned to the reaction centre. Or it can be non-cyclic, in
environmental change through time. which case a new electron must be found to restore the reac-
I will focus on one example, the evolution of oxygenic tion centre pigment (see Falkowski & Raven, 1997, for a thor-
photosynthesis, that exemplifies how evolutionary innovations ough review of light reactions in photosynthesis).
inferred from comparative biology and planetary history Most photosynthetic bacteria have a single photosystem
drawn from palaeontology and geochemistry can illuminate linked to an electron transport chain containing either Fe-
some principal issues in geobiology. I choose this example quinones or FeS proteins. Electron resupply comes from
because the supporting facts are reasonably well known (if not H2S, S2O3=, H2, organic molecules, or even Fe2+, and oxygen
universally agreed upon), increasing, I hope, the transparency does not enter the picture. Cyanobacteria are unique among
of the approach I wish to illustrate. I will also consider, at least photosynthetic bacteria because they contain two coupled
briefly, whether the mechanistic processes of evolutionary photosystems. H2O provides the electrons needed for photo-
biology principally those of population genetics generally synthesis, and O2 is generated as a by-product. Interestingly,
contribute to change or stasis in the Earth system. in cyanobacteria, the coupled photosystems differ from one
another: photosystem II contains Fe-quinones, like those of
proteobacteria and green non-sulphur bacteria, whereas
THE EVOLUTION OF PHOTOSYNTHESIS AND
photosystem I uses FeS proteins like those of green sulphur
ITS GEOBIOLOGICAL CONSEQUENCES
bacteria and heliobacteria. This suggests that cyanobacterial
If there is one fact that every geophysicist knows about biology photosynthesis, with its capacity for oxygen generation, evolved
it is that photosynthesis generates the oxygen that makes air from pre-existing anoxygenic phototrophs by lateral transfer
breathable. At one level, this observation is indisputable in of a photosystem gene cassette (Blankenship, 1992).
the absence of oxygenic photosynthesis Earths atmosphere Of course, more than lateral transfer was needed to assem-
could not contain 21% O2 by volume, and were oxygenic ble the two photosystems coupled in cyanobacteria. Oxygenic
photosynthesis to be suspended, the atmospheric reservoir of photosynthesis required reaction centre molecules with a
oxygen would decay over an interval of several million years. standard potential sufficient to drive the oxidation of water
But let us ask two slightly different questions. (1) What is a good case can be made for the evolution of chlorophyll a
the historical relationship between the evolutionary innova- from bacteriochlorophyll g, found in the closely related helio-
tion of oxygenic photosynthesis and the changing redox state bacteria (Kobayashi et al., 1998). It also required the evolu-
of the atmosphere and oceans? Was the oxidation of the bio- tion of a molecular complex at the front end of photosystem
sphere the inevitable and immediate consequence of photo- II that can bind H2O and extract the electrons needed to
synthetic innovation, or is there more at issue? (2) To the replace those lost by photon excitation. Buchel et al. (1999)
extent that evolution and environmental history are linked, have recently proposed that a manganese bicarbonate complex
does the vector of causation run in only one direction? Or, has originally provided electrons for photosynthesis, eventually
atmospheric change itself influenced the continuing evolution giving rise to the Mn-catalysed protein complex that splits
of photosynthetic organisms? water to produce both electrons and oxygen in present-day
cyanobacteria. Finally, an entirely different set of reactions was
needed the so-called dark reactions that fix carbon dioxide
The biology of photosynthesis
to form sugar, using the ATP and reducing power generated
First, we must understand the biological innovation in question. by light reactions. Carbon fixation in cyanobacteria proceeds
It was not the evolution of photosynthesis. The use of solar via the familiar CalvinBenson cycle, as it does in photo-
energy to drive the reduction of carbon dioxide and generate synthetic proteobacteria. Other photosynthetic bacteria, how-
ATP evolved early within the bacteria. At least five major ever, employ quite different molecular pathways to fix CO2
bacterial clades (cyanobacteria, proteobacteria, heliobacteria, (Fuchs & Stupperich, 1985).
green sulphur bacteria, and green non-sulphur bacteria) include The preceding comments only hint at the molecular com-
photosynthetic organisms, and four of these do not produce plexity of photosynthesis, but they suffice to show that oxy-
oxygen as a by-product (Blankenship, 1992). genic photosynthesis is an intricate construction that unites
In all photosynthetic bacteria, pigments (chlorophyll or several distinct molecular innovations to form a unique func-
bacteriochlorophyll, plus accessory pigments) absorb photons tional system. From an ecological perspective, this concatena-
of light. Within the photosynthetic reaction centre, each tion might well be regarded as the central event in the history
photons energy is transferred to an electron, which leaves its of life, because it liberated biology from hydrothermal vents

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Geological consequences of evolution 5

Fig. 1 Proterozoic microfossils reliably interpreted


as cyanobacteria. (A) Eohyella, a fossil counterpart
of the extant endolithic cyanobacterium Hyella,
preserved in silicified ooids from the Neoproterozoic
LimestoneDolomite Series, East Greenland; (B)
A species of the modern cyanobacterial genus
Entophysalis, from Shark Bay, Australia, for com-
parison with C (photo by John Bauld). (C) Eoento-
physalis, a mat-forming colonial cyanobacterium
from silicified tidal flat carbonates of the early
Mesoproterozoic Bil-yakh Group, northern Siberia.
(D) Polybessurus, fossil counterpart of extant
Cyanostylon-like cyanobacteria, preserved in silicified
tidal flat carbonates from the Neoproterozoic
Draken Formation, Spitsbergen. Scale bars in B =
125 m for A, and 30 m for BD.

and other environments where locally strong redox gradients The palaeobiological question is: how can we identify a
could support chemosynthetic life, allowing organisms to cyanobacterial signature in sedimentary rocks? Microfossils
spread across the planet (Knoll & Bauld, 1989). And it only provide an obvious means of addressing this question. In terms
happened once. The green-plant photosynthesis found in of morphology, cyanobacteria are among the most diverse of
algae and land plants is explained by another form of lateral all bacteria, and while some cyanobacteria are simple and have
transfer the incorporation into eukaryotes of entire cyano- forms replicated widely among bacteria, others have morpholo-
bacterial cells (Margulis, 1981; Delwiche, 1999). gies not known in other bacterial clades (Geitler, 19301932).
Thus, the distinctive morphology and behaviour of endoliths
such as Hyella is unambiguous when observed in Proterozoic
The antiquity of oxygenic photosynthesis
fossils from East Greenland (Green et al., 1988; Fig. 1A). The
Did the innovation of oxygenic photosynthesis translate directly same is true of the cushions of stalked Cyanostylon-like fossils
and immediately into an oxic atmosphere and oceans? To commonly found in chert nodules within Neoproterozoic
address this, we must ask palaeontologists when cyanobacteria tidal flat carbonates (Green et al., 1987; Fig. 1D).
evolved, and compare that estimate with the history of The oldest fossils that have a morphology diagnostic for
atmospheric oxygen inferred from geochemical proxies. cyanobacteria are Entophysalis-like colonies preserved in

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6 ANDREW H. KNOLL

c. 2000 Ma cherts from the Belcher Islands, Canada (Golubic that observed fractionation records the additive efforts of car-
& Hofmann, 1976; Hofmann, 1976; Fig. 1B,C). Earlier ento- bon fixation by the reductive citrus acid cycle (812) and
physalids may occur in 2500 Ma cherts of the Transvaal Super- secondary fractionation associated with methanogenesis and
group, South Africa, but poor preservation limits confidence methanotrophy (Knoll & Canfield, 1998). Indeed, recent
in this interpretation (Altermann & Schopf, 1995). Older reinterpretations of reduced carbon in Early Archean rocks
microfossils are not only rare and contentious, they do not raise the spectre that non-biological C-isotopic fractionation
have morphologies that are diagnostic for cyanobacteria. We might have been important on the early Earth. C-isotopic frac-
must be particularly aware of this when we attempt to interpret tionation associated with FischerTropsch and other abiolog-
putative microfossils in nearly 3.5 Ga rocks of the Warrawoona ical processes tends to be strongly condition dependent
Group, Australia (Schopf & Packer, 1987; Schopf, 1992), and (Chang et al., 1983). In consequence, varying concentrations
elsewhere (Walsh, 1992; Knoll & Barghoorn, 1977; Walsh & of reactants might lead to variable 13Corg where abiological
Lowe, 1999; Rasmussen, 2000). If biological at all (Brasier processes were prominent parts of the carbon cycle. Graphite
et al., 2002; Schopf et al., 2002), these do not possess features from phosphate granules in the 3.8 Ga Akilia gneisses of
that can be used to constrain physiology. There is no compel- south-western Greenland varies by as much as 40 (Mozjsis
ling reason to interpret them as cyanobacterial. et al., 1996; see also Van Zuilen et al., 2002), which, if unre-
What about stromatolites, generally interpreted as the trace lated to measurement technique (Hayes, 1996), is consistent
fossils of cyanobacterial mat communities? Paralleling the with such a prediction. On the other hand, isotopic measure-
microfossil record, many Proterozoic stromatolites preserve ments of reduced carbon from broadly correlative but less
petrological fabrics indicative of cyanobacterial participation highly altered metasediments in the Isua region show only
in lamina accretion (e.g. Bertrand-Sarfati, 1976; Knoll & limited variation (Rosing, 1999). The same holds for organic
Semikhatov, 1998). Nearly all of these formed by the trapping carbon in 3.43.5 Ga rocks from the Onverwacht Group,
and binding of fine-grained sediments by microbial com- South Africa, and the Warrawoona Group (Strauss & Moore,
munities. More problematic are stromatolites that accreted by 1992). These data, sketchy as they are, provide our best cur-
the repeated precipitation of mineral laminae. We know that rent evidence for early autotrophy. Clearly, however, they
microbial mats can facilitate carbonate precipitation, but place only limited constraints on the nature of Early Archean
other processes can do so as well, making the biological inter- physiologies.
pretation of precipitated stromatolites difficult (Grotzinger More persuasive evidence for cyanobacteria comes from
& Rothman, 1996). For example, silicified Palaeo- and Meso- >C31 2-methylhopanes (2Me-hopanes) recovered from
proterozoic carbonates show that the microdigitate stromato- 2.7 Ga bitumens in north-western Australia (Brocks et al.,
lites common in rocks of this age consist of stacked crystal fans 1999). Summons et al. (1999) showed that that many cyano-
whose relationship to microbiology in general and cyanobac- bacteria synthesize 2-methylbacteriohopanepolyol (2-MeBHP),
teria in particular is difficult to establish (Hofmann & Jackson, the precursor compound to the 2Me-hopanes. Indeed, only
1987). The problem, as John Grotzinger first recognized, is cyanobacteria are known to produce this compound in con-
that as we recede further back in time, the ratio of precipitated centrations likely to account for its abundance in Precambrian
to trapped and bound stromatolites increases. In consequence, sedimentary rocks. Nonetheless, geological interpretation
the proportion of stromatolitic structures that can be inter- turns on the phylogenetic distribution of 2-MeBHP synthesis,
preted with confidence as products of cyanobacterial commu- which remains incompletely known. It appears that not all
nities declines with age (Grotzinger & Knoll, 1999). cyanobacteria produce 2-MeBHP (Summons et al., 1999). If
Stromatolites occur in Early Archean successions, and, this biosynthetic capability evolved only within derived line-
not surprisingly, their interpretation is controversial (Buick ages of cyanobacteria, we are in good shape in this case oxy-
et al., 1981; Lowe, 1994). In some cases, especially the conical genic photosynthesis must have evolved before the ability to
structures found in 3.45 Ga rocks of the Warrawoona Group synthesize 2-MeBHP, and 2-Me-hopanes can be used as geo-
(Hofmann et al., 1999), accretion may have been facilitated logical proxies for oxygenic photoautotrophs. If, however,
by micro-organisms, but the case for cyanobacterial involve- 2-MeBHP occurred in the last common ancestor of all cyano-
ment remains to be made. bacteria, then we have no way of knowing whether coupled
If fossils and stromatolites fail us, what about carbon iso- photosystems or 2-MeBHP arose first along the evolutionary
topes? These provide some of our deepest historical insights pathway to modern cyanobacteria. Unless the two traits orig-
into metabolism, and certainly the fractionation observed inated simultaneously, stem group cyanobacteria could have
in reduced carbon as old as 3.8 Ga is consistent with CO2 fix- featured 2-MeBHP synthesis but not oxygenic photosynthe-
ation via the CalvinBenson cycle (Rosing, 1999). But, as noted sis, or vice versa, and should abundant 2-MeBHPs be found
above, proteobacteria as well as cyanobacteria fix carbon this way. in heliobacteria or other clades, the interpretational difficulties
Moreover, it is difficult to rule out the possibility that Early will spiral.
Archean carbon was fixed via the reductive acetyl coenzyme A So, the antiquity of oxygenic photosynthesis is, in fact, dif-
pathway, which fractionates C-isotopes by up to 34 40, or ficult to establish. The presence of steranes in the same 2.7 Ga

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Geological consequences of evolution 7

Fig. 2 Geological time-scale showing palaeontological and geochemical constraints on the antiquity of oxygenic photosynthesis (cyanobacteria), as well as the
inferred redox history of the oceans and atmosphere. Phanero = Phanerozoic Era. See text for discussion and references.

shales that contain 2-Me-hopanes provides further, inferential that the atmosphere generated by early outgassing was neutral
support for the antiquity of oxygenic photosynthesis because to mildly reducing and that it did not become strongly or
the sterols from which these steranes were derived require persistently oxidizing for some two billion years (for a dissenting
molecular oxygen for their synthesis (Jahnke & Klein, 1983). view, see Ohmoto, 1996).
The required partial pressures of oxygen are not high and Traditionally, arguments about oxidation history have relied
could have been restricted to local oxygen oases (Knoll, 1999). on the temporal distributions of detrital uraninite, pyrite,
Nonetheless, if we can rule out contamination by younger siderite and banded iron formation (Cloud, 1968; Holland,
materials, the simultaneous presence in 2.7 Ga bitumens of 1984; Rasmussen & Buick, 1999). Uraninite, siderite and
steranes and 2-Me-hopanes suggests that cyanobacteria were pyrite all oxidize readily in the presence of oxygen. Thus, their
present in Late Archean ecosystems (Fig. 2). Further support- accumulation as detrital grains in well-aerated fluvial sedi-
ive evidence for this conclusion comes from similarly ancient ments deposited before c. 2.42.2 Ga and their rarity thereaf-
stromatolites with palimpsests of phototrophic microbes that ter implies low oxygen concentrations in Archean and earliest
occur in sulphate-deficient lakes formed on basalt basement Proterozoic air. Holland and colleagues (e.g. Rye & Holland,
(Buick, 1992). No metabolic reagents other than CO2 and 1998) have added palaeosol chemistry to the mix, arguing that
H2O were available in these restricted evaporitic basins, so the Fe released by chemical weathering will be lost when ground
only plausible method of primary production was oxygenic waters are anoxic, but retained quantitatively when ground
photosynthesis by cyanobacteria. waters carry oxygen. Weathering horizons developed before
Of course, cyanobacteria may have evolved much earlier. 2.4 Ga show substantial iron loss, whereas younger palaeosols
Nothing in the earlier record precludes an Early Archean retain weathered iron (Beukes et al., 2002).
origin of oxygenic photosynthesis it is just that nothing we Still more recently, sulphur isotopes have been brought to
know at present requires such an early origin. bear on questions of Archean redox conditions. Cameron
(1982, 1983) demonstrated two decades ago that S-isotopic
fractionation in marine basins increased early in the Protero-
The geobiological consequences of oxygenic photosynthesis
zoic Eon (Figs 2 and 3). Insofar as the environmental factor
When, then, did Earths atmosphere turn oxic? Debate about most likely to affect fractionation is sulphate availability
the Archean atmosphere continues, but most workers accept (Habicht & Canfield, 1996), Canfield and colleagues

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8 ANDREW H. KNOLL

Fig. 3 Diagram showing general patterns of secular variation in C and S isotopes through Archean and Proterozoic time, along with a broad estimate of atmospheric
oxygen levels. a denotes relatively high S-isotopic fractionation observed in evaporitic facies (but not open water deposits) of the 3.45 Ga Warrawoona Group
(Shen et al., 2001). See text for discussion and references.

(Canfield & Teske, 1996; Canfield & Raiswell, 1999; Canfield inventory, because it appears that oxygen began to approach
et al., 2000) interpret this pattern in terms of a growing oce- its modern state only much later in Earth history (Knoll et al.,
anic sulphate reservoir related to increasing oxygen in the 1986; Derry et al., 1992; Knoll, 1992; Canfield & Teske,
atmosphere and surface ocean. Consistent with this view, an 1996; Shen et al., 2002a). Banded iron formations disap-
early Palaeoproterozoic decline in organic carbon character- peared at c. 1700 Ma, requiring that substantial portions of
ized by unusual 13C depletion appears to record a global the deep ocean remained anoxic well after 2400 Ma. And Can-
decline in the importance of methanogenesis in the recycling field (1998) has proposed that, when it occurred, the cessation
of marine organic matter (Hayes, 1994; Des Marais, 1997). of iron deposition recorded not the oxidation of deep waters
Mass-independent S-isotopic fractionation also supports but rather the growth of a sulphate reservoir sufficient to drive
the idea of low pre-Proterozoic oxygen tensions. Farquhar sulphate reduction at rates capable of removing iron by reaction
et al. (2000) detected mass independent fractionation of with H2S. According to Canfield, then, the mid-Proterozoic
sulphur isotopes in sedimentary sulphur species formed before deep ocean was predominantly sulfidic, not oxic.
c. 2.4 Ga but not after about 2.1 Ga. They propose that this Geochemical tests of this hypothesis are few, but growing.
pattern reflects the transition from a sulphur cycle governed by Shen et al. (2002) examined S-isotopes and Fe-speciation
photochemical processes in an oxygen-free atmosphere to one chemistry of c. 1730 Ma and 1640 Ma black shales deposited
dominated by oxidation during continental weathering and during maximum flooding events in the northern Australian
biological processes in the oceans. Tawallah and McArthur groups, respectively. Iron chemistry
Thus, a case can be made that oxygen tensions increased suggests deposition beneath anoxic bottom waters, as occurs
globally at c. 2.4 Ga. This establishes a firm minimum date for today in the Black Sea. Also, the limited fractionation and low
the origin of cyanobacterial photosynthesis, but, as noted variance displayed by S-isotopes in sedimentary pyrites from
above, blue-greens likely existed at least 300 Ma earlier, and Tawallah and McArthur shales suggest (a) that much sulphate
they may have evolved long before than that. Regardless of reduction occurred in the water column and (b) that sulphate
when oxygenic photosynthesis began, however, it cannot pro- was substantially depleted in these deep waters requiring that
vide a sufficient explanation for Earths current atmospheric well into the Proterozoic, sulphate reservoirs were much lower

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Geological consequences of evolution 9

than today. Continuing research by Shen et al. (2003) shows many have recognized (e.g. Godderis & Veizer, 2000). Exactly
that basinal black shales of the < 1500 Ma Roper Group also what processes modulated the historical accumulation of
record anoxic deep waters and low sulphate abundances. Both oxygen in the atmosphere and oceans remains a subject for
deep water anoxia and low sulphate abundance can be local debate; recent proposals (not mutually exclusive) include
rather than global features of preserved basins. Australian data hydrogen escape after methane photolysis in the upper atmos-
indicate that in this one corner of the world, however, low phere (Catling et al., 2001), phosphate limitation of primary
oxygen and low sulphate characterize preserved basinal succes- production in early oceans (Bjerrum & Canfield, 2002) and
sions through some 250 million years of mid-Proterozoic his- small changes in the oxygen fugacity of the mantle that
tory. Independent studies by Lyons et al. (2000) in the Belt resulted in less reduced gas fluxes from volcanoes (Holland,
Supergroup and Kah et al. (2001) in younger Mesoprotero- 2002). It is further unclear why PO seems to have remained
2
zoic successions from Baffin Island also suggest that mid- at least broadly stable over long intervals of time. This, I sus-
Proterozoic sulphate levels were low relative to todays. pect, is where we should seek biological control mechanisms.
Indeed, increasing data support the hypothesis that modern In any event, the role of photosynthesis is clear. Oxygenic
sulphate and oxygen levels may only have been approached photosynthesis was absolutely necessary for the development
near the end of the Proterozoic, just before the Ediacaran and maintenance of Earths contemporary atmosphere. Yet,
radiation (Hurtgen et al., 2002). Until late in the Proterozoic what evolution did in this case was define the dimensions of
Eon, maximum S-isotopic fractionation rarely if ever exceeded biological participation in the Earth system. It was the inter-
the upper limit of 45 associated with bacterial sulphate action of biological processes with tectonics that determined
reduction (Canfield & Teske, 1996; Fig. 3). The larger frac- the state of the system through time.
tionations (up to 70) found in Phanerozoic sedimentary
rocks originate when sulphur compounds formed by the oxi-
OXYGEN AND THE CONTINUING
dation of hydrogen sulphide undergo disproportionation to
EVOLUTION OF PHOTOSYNTHETIC
produce sulphate and sulphide. Canfield (1998) argued that
ORGANISMS
we do not see these larger fractionations in older Proterozoic
successions because hydrogen sulphide generated in anoxic What about my second question? Has the continuing
deep waters was taken up by anoxic photoautotrophs before it oxidation of the Earth surface system influenced the ongoing
came into contact with oxygenated surface waters that in most evolution of photosynthetic physiology? Unambiguously, the
Proterozoic oceans the redoxcline fell within the photic zone. answer is yes.
By extension, the prominence of larger fractionation in succes- Rubisco, the key enzyme responsible for CO2 fixation in
sions deposited during the past 600 million years suggests that oxygenic photoautotrophs, evolved early in Earth history when
since this time, oceans have been more fully oxygenated. PCO2 was high and PO2 negligible. This would be of limited
The abundance and distribution of oxygen in Proterozoic relevance were it not for the fact that Rubisco functions as
oceans remains contentious, as does the timing and mecha- an oxygenase as well as a carboxylase. That is, oxygen com-
nism of proposed Neoproterozoic increase in O2 levels (e.g. petes with CO2 for binding sites in the Rubisco molecule
Anbar & Knoll, 2002). Nonetheless, it appears increasingly (Larcher, 1983). In consequence, as PO has increased through
2
likely that although the innovation of oxygenic photosynthesis time and PCO declined, the oxygenase capacity of Rubisco has
2
occurred once, early in our planets history, the oxidation of become more and more of a physiological burden, eroding the
the oceans and atmosphere was a protracted affair that played net photosynthetic capacity of cyanobacteria, algae and land
out episodically over two billion years (Figs 2 and 3). plants (Larcher, 1983).
Why is there this historical mismatch? Why didnt the evo- Photosynthetic organisms have evolved several distinct
lution of oxygenic photosynthesis rapidly engender an oxygen- responses to these changing environmental circumstances.
rich biosphere? In no small part, of course, it is because First, photoautotrophs have evolved an elaborate biochemical
oxygenic photosynthesis forms a tight metabolic redox couple pathway (involving, in photosynthetic eukaryotes, the mito-
with aerobic respiration. Moreover, oxygen is also consumed chondria and peroxisomes, as well as chloroplasts) for salvag-
by reaction with minerals and reduced volcanic gases (com- ing the products of RuBP oxidation. Known as photorespiration,
monly mediated by micro-organisms). In geological time, this pathway returns carbon to the CalvinBenson cycle, albeit
then, oxygen fluxes to the atmosphere will reflect not gross at some energetic cost (Larcher, 1983). Second, photosyn-
photosynthesis, but the net balance between oxygen produc- thetic organisms have evolved several mechanisms to limit the
tion and oxygen consumption by aerobic respiration and in vivo oxygenase activity of Rubisco. Photosynthetic bacteria,
oxidation of inorganic materials. algae and land plants show marked phylogenetic variation
Because organic carbon burial effectively decouples photo- in the chemical affinity of Rubisco for CO2 and in the degree
synthesis and respiration, and because mid-oceanic ridges and to which given oxygen tensions affect rates of CO2 fixation
volcanoes supply reduced gases to the Earth surface system, later evolving groups fix carbon more effectively in the face of
tectonics assumes a driving role in atmospheric history, as ambient oxygen (Raven, 1997).

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10 ANDREW H. KNOLL

Also, many photoautotrophs have carbon concentrating substrates for another, and further constraints arise from the
mechanisms that maintain locally high CO2/O2 within cells. interactive nature of biogeochemical cycles. Biological participa-
Many algae pump bicarbonate across the cell membrane, con- tion in the Earth system may be governed by photosynthesis,
verting it to CO2 within the cell (Kaplan & Reinhold, 1999; but photosynthesis itself is modulated by the availability of
Ghoshal & Goyal, 2001). Vascular plant adaptations include fixed nitrogen, phosphorus and trace nutrients (Sterner & Elser,
C4 photosynthesis, in which CO2 is fixed into the four carbon 2002). This codependence of elemental cycles must help to
compounds oxaloacetate or malate by PEPcarboxylase, trans- buffer the environmental effects of metabolic innovation.
ported to specialized cells surrounding vascular tissues, released Third, structural as well as physiological innovations in pho-
enzymatically by decarboxylation, and, finally, refixed via tosynthetic organisms may affect the Earth system, but are
Rubisco to enter the Calvin-Benson cycle (Larcher, 1983; most likely to do so if they result in a departure from the
Leegood, 2002). C4 photosynthesis, thus, ensures locally high C:N:P ratios common to most organisms. In geological time,
CO2/O2 in cells where Rubisco is active; CAM plants such as such departures have been rare; perhaps the best example is
cacti do much the same thing, but segregate the two pathways wood, which contains C, but not N or P. As Berner (1998)
of CO2 fixation in time rather than in space (Larcher, 1983). and others have argued, the evolutionary emergence of woody
Photorespiration and carbon-concentrating mechanisms, seem- plants, with its consequences for the increased penetration of
ingly the constructs of some biological Rube Goldberg, find substrates by roots and the new reservoir of metabolically
evolutionary interpretation as responses to biospheric oxygen- recalcitrant organic particles in soil and sediments, coincides in
ation necessitated by the functional constraints of Rubisco. time with an inferred late Palaeozoic decrease in PCO2 and may
have been its proximal cause. At the same time, the oxygen
generated by photosynthesis has affected the continuing evo-
AN ATTEMPT AT GENERALIZATION
lution of photosynthetic organisms. On the road connecting
The foregoing discussion prompts several summary thoughts, evolution and environment, traffic flows in both directions.
at least some of which may point toward general features of the
relationship between evolutionary innovation and environmental
EVOLUTIONARY PROCESS IN
change.
ENVIRONMENTAL HISTORY
First, innovations in metabolism define the dimensions of
biological participation in the Earth system, but they seldom Having explored, through one example, the relationship
determine the state of the system by themselves. Rather, each between evolutionary innovation and environmental change,
metabolism interacts with other components of the system to we need to ask about another relationship, that between
determine its state. evolutionary process and environmental history. Two iconic
Second, the redox coupling of nearly all important meta- representations of biology help us to think about an answer.
bolic pathways places an important constraint on the capacity The first is a powerful evolutionary metaphor originally
of metabolic innovation to drive Earth system state change. developed by Sewall Wright (1932): the adaptive landscape
The products of a given metabolism nearly always provide (Fig. 4A). In Wrights conception, each point on the landscape

Fig. 4 Two iconic representations of biology: (A) the adaptive landscape, as illustrated by Wright (1932); (B) Daisyworld simulation of planetary temperature
regulation by daisies with differing albedos, as depicted by Lovelock (1989). See text for discussion.

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Geological consequences of evolution 11

surface represents a specific genotype; elevations reflect the maintain the planetary surface close to the optimal tempera-
relative fitness of different genotypes in a specified environment. ture for daisy growth as solar luminosity increases. The exper-
Because of natural selection, new colonists placed in the iment ends when solar luminosity exceeds the buffering
landscape will tend to climb the nearest adaptive peak (not capacity of daisies, as dictated by their maximum growth
necessarily the highest one), quickly, in evolutionary terms, temperature of 40 C.
gaining its summit. Once a peak is occupied, the likelihood Daisyworld owes its regulatory power to the fact that it
that further mutation will result in improved fitness declines to specifies a fixed set-point, the optimum temperature for daisy
zero. In consequence, subsequent selection is largely stabilizing, growth (Weber, 2001). In its original, explicitly ecological form,
acting to maintain the successful population see, for example, this assumption seems reasonable, but what happens when we
Lenski & Travasianos (1994) experimental studies of allow daisies to mutate and adapt? Robertson & Robinson (1998)
adaptation in E. coli. While the environment remains steady, modelled a Daisyworld in which evolving daisies shifted their
stasis including the now classical palaeontological stasis of optimal growth temperature to match their local environ-
Gould & Eldredge (1993) will be favoured. (Radical ment. In consequence, the bioregulation observed in purely
mutations may allow populations to jump from one adaptive ecological models broke down (see also Lansing et al., 1998).
peak to another, but the chances of that happening in an Such simulations suggest that, by itself, system-dependent
ecologically full world are small.) selection will not predictably endow ecosystems with negative
What happens, then, when a genotype contributes to feedbacks. Other homeostatic mechanisms must be afoot.
change in its surrounding environment? In an altered fitness Nonetheless, the parable of Daisyworld suggests two sensible
landscape, the genotype is likely to fall on an adaptive slope or conclusions. First, when applied at the right scale required by
valley rather than a peak. That is, changing the ambient envir- both population genetics and physical interactions to be local
onment has an evolutionary effect not dissimilar to deleterious not global (Weber, 2001; see Daly & Smith, 1993, for a real
mutation, decreasing the fitness of genotypes that formerly world example) Daisyworld suggests that biological variation
occupied adaptive peaks. It might seem therefore that selec- helps to buffer externally imposed environmental change.
tion should act to sustain genotypes best able to maintain Second, the buffering capacity is limited. When extrinsic
local environmental stasis. There is, however, a wrinkle to environmental forcing exceeds a certain threshold, homeostasis
this argument. While an altered adaptive landscape will pro- fails and the system moves to a new state. Ice ages illustrate the
bably decrease the fitness of genotypes that were maximally point.
fit before, it may increase the fitness of other genotypes present How, then, does the Earth system remain within a relatively
in the population. That is, environmental change engendered narrow range of variation for long time intervals? The biological
by one genotype (or population or species) may well benefit a processes that contribute most effectively to environmental
second genotype. This, of course, is just what happens among homeostasis are probably those mentioned earlier as con-
species during ecological succession (e.g. Lenton, 1998). straints on the environment impact of evolutionary innova-
Lansing et al. (1998) termed this response system-dependent tions: the linkage of complementary metabolisms in
selection and argued that it will increase environmental regula- biogeochemical cycles and systems (Tateno & Chapin, 1997;
tion by the biota. I suspect that in the presence of biological Downing & Zvirinsky, 1999). If photoautotrophs deplete
variation, population genetics will commonly act as a buffer ambient CO2, biologys most potent response is to decrease
against biologically induced environmental change, but the rates of photosynthesis while increasing respiration to restore
buffer is weak and I have no confidence it will hold on evo- carbon dioxide. Rates of growth and metabolism provide
lutionary time-scales. more sensitive controls on environmental homeostasis than
This prompts consideration of a second icon, the Daisy- population genetics.
world model of biological control in the Earth system Of course, population genetic processes produce evolution-
(Fig. 4B). In early formulations (e.g. Watson & Lovelock, ary innovations, and, as exemplified by the origin of wood,
1983), Daisyworld is seeded in proximity to a sun whose lumi- these may facilitate environmental state change. The geologi-
nosity increases through time. Initially, the temperature of cal record, however, suggests that more commonly the vector
Daisyworld is less than 5 C, the minimum temperature for of causation has pointed in the other direction that the alter-
daisy growth. As solar luminosity, and, hence, surface temper- ation of fitness landscapes by imposed environmental change
ature, increase, daisies begin to germinate, influencing the has facilitated evolutionary innovation. (I do not mean to
ambient environment as they grow by altering the planets imply that evolution occurs only in response to changes in the
albedo. All daisies grow best at 22.5 C, but dark and light physical environment. Evolutionary change commonly reflects
individuals differ in their capacity to absorb sunlight. In con- changes in the biological components of a species effective
sequence, dark daisies are initially at an advantage and spread environment.) With change in the physical environment,
to cover the planet, warming it as they go. As solar luminosity dominant genotypes and populations have disappeared, and
increases, however, light daisies will begin to expand, and the survivors and new colonists climbed emerging adaptive peaks.
changing mixture of dark and white individuals will act to This is what happened when oxygen invaded the atmosphere.

2003 Blackwell Publishing Ltd, Geobiology, 1, 3 14


12 ANDREW H. KNOLL

It is what happened when decreasing CO2 and increasing O2


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