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CHAPTER 8

The Geological Succession of Primary Producers in the Oceans

ANDREW H. KNOLL, ROGER E. SUMMONS, JACOB R. WALDBAUER, AND JOHN E. ZUMBERGE

I. Records of Primary Producers in Ancient Oceans A. B. Molecular Biomarkers II. The Rise of Modern A. and Phylogeny B. Biomarkers and the Rise of Modern Phytoplankton C. Summary of the Rise of Modern Phytoplankton III. Primary Production A. Microfossils B. Paleozoic Molecular Biomarkers C. Paleozoic Summary IV. Primary Production A. Prokaryotic Fossils B. Eukaryotic Fossils C. Proterozoic Molecular Biomarkers D. Summary of the Proterozoic Record V. Oceans VI. Conclusions A. Directions for Continuing Research References

In the modern oceans, , dinoflagel- geobiological prominence only in the lates, and coccolithophorids play prominent Era also requires that other primary producers roles in primary production (Falkowski et al. fueled marine ecosystems for most of Earth 2004). The biological observation that these history. The question, then, is What did pri- groups acquired via endo- mary production in the oceans look like before symbiosis requires that they were preceded in the rise of modern phytoplankton groups? time by other photoautotrophs. The geologi- In this chapter, we explore two records cal observation that the three groups rose to of past primary producers: morphological

133

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fossils and molecular biomarkers. Because without well developed might these two windows on ancient are well leave no morphologic record at all in framed by such different patterns of pres- sediments. ervational bias and diagenetic selectivity, By virtue of their decay-resistant extracel- they are likely to present a common picture lular sheaths and envelopes, many cyano- of stratigraphic variation only if that view have a relatively high probability reflects evolutionary history. of entering the record, and some ben- thic lineages are both readily preservable I. RECORDS OF and morphologically distinctive (Knoll and PRIMARY PRODUCERS Golubic 1992). On the other hand, impor- IN ANCIENT OCEANS tant such as Prochlorococcus are unlikely to leave recognizable body (or, as A. Microfossils it turns out, molecular) fossils. A number of algal include good candidates for fos- Microfossils, preserved as organic silization, especially groups with distinctive walls or mineralized tests and scales, record resting stages (phycomate prasinophytes, the morphologies and (viewed via transmis- ) or mineralized skeletons sion electron microscopy) ultrastructures of (diatoms, coccolithophorids, coralline reds, ancient . Such fossils can caulerpalean and dasyclad greens). Other provide unambiguous records of phyto- primary producers fossilize occasionally, but in past oceans— frustules, only under unusual depositional or diage- for example—and they commonly occur netic circumstances (e.g., Butterfield 2000; in large population sizes, with numerous Xiao et al. 2002, 2004; Foster and Afonin 2006), occurrences that permit fine stratigraphic and still others rarely if ever produce mor- resolution and wide geographic coverage. phologically interpretable fossils. Set against this is a number of factors Diagenesis can obliterate fossils as well that limit interpretation. Not all photoau- as preserve them: organic walls are subject totrophs produce preservable cell walls or to post-depositional oxidation and min- scales, and, of those that do, not all gener- eralized skeletons may dissolve in under- ate fossils that are taxonomically diagnos- saturated pore waters. The result is that tic. Thus, although many modern diatoms presence and absence cannot be weighted precipitate robust frustules of silica likely equally in micropaleontology. The presence to enter the geologic record, others secrete of a fossil unambiguously shows that the weakly mineralized shells with a corre- cell from which it derived lived at a certain spondingly lower probability of preserva- time in a particular place, but absence may tion. Similarly, whereas dinoflagellates as a reflect true absence, low probability of fos- group have left a clear record of , silization, or obfuscating depositional or many extant species do not produce pre- diagenetic conditions. For older time inter- servable cysts and others form cysts that vals, tectonic destruction of the sedimentary would not be recognized unambiguously record imposes an additional challenge; in as in fossil assemblages. (The particular, subduction inexorably destroys phylogenetic affinities of fossil dinocysts oceanic crust and the sediments that mantle are established by the presence of an arche- it, so that deep sea sediments are common opyle, a distinctive excystment mechanism only in and younger ocean basins. peculiar to but not universally found within dinoflagellates.) Especially in the early his- B. Molecular Biomarkers tory of a group, character combinations that readily distinguish younger members may The chemical constituents of biomass pro- not be in place. Thus, stem group diatoms duced by living can be incorporated

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into sediments and ultimately into sedimen- can remain recognizable as the products of tary rocks that can survive for billions of . particular biosynthetic pathways on time Where these compounds are preserved in scales that approach the age of the Earth recognizable forms, they represent another (e.g., Brocks and Summons 2004; Peters opportunity for organisms to leave a trace et al. 2005). of themselves in the fossil record. Organic The character of the information con- biomarkers are the diagenetically altered tained in molecular fossils is variable. Some remains of the products of cellular biosyn- are markers for the presence and, to the thesis and may be aptly termed molecular extent they can be quantified relative to other fossils. Most biomarkers are derived from inputs, abundance of particular organisms. lipids and are potentially stable over bil- The taxonomic specificity of such biomar- lion- time scales under ideal conditions kers ranges from species to level. (Brocks and Summons 2004). Others are markers for the operation of a Given the variety of organic compounds particular physiology or biosynthetic path- produced by cells, and the vast quantities of way that may have a broad and/or patchy sedimentary organic matter in a rock record taxonomic distribution. Still other kinds of that stretches back billions of years, biomar- biomarkers are most strongly associated kers are a potentially rich source of informa- with specific depositional settings, making tion concerning the diversity and ecology of their presence more indicative of paleoen- ancient communities. However, the process vironmental conditions than of any particu- of organic matter incorporation into rocks lar biology. Interpretation of the molecular and its transformation during deep burial fossil record depends on our ability to rec- imposes some strong constraints on the ognize biomarker compounds, link them to kinds of information that can be recovered biosynthetic precursors, and then to make millions of years after the fact. The classes of inferences about what the presence of those molecules that contain molecular sequence molecules in the rock record tells us about information, nucleic acids and most pro- contemporary biology and geochemistry. teins, do not survive long in the geologic Turning to biomarkers that might estab- environment. DNA can survive for at least lish a molecular fossil record of primary pro- a few hundred thousand years, especially in duction in marine settings, several classes reducing environments such as euxinic sed- of compounds are promising for their com- iments (e.g., Coolen et al. 2004) where het- bination of biochemical and/or taxonomic erotrophy is curtailed by a lack of electron specificity. Pigments are natural candidates, acceptors but is not an option where the representing markers of the photosynthetic aim is to look at changes on million-year or machinery itself. Input of to longer time scales. Other kinds of biomol- sediments can result in several kinds of ecules, however, prove remarkably resilient molecular fossils, including porphyrins in the rock record. and the pristane and phytane skeletons of Any molecule with a hydrocarbon skel- the chlorophyll side-chain (Figure 1). It was eton has the potential to be preserved the recognition of vanadyl porphyrin as over long periods. For the most part, this the molecular fossil of chlorophyll that led means the hydrocarbon portions of mem- Alfred Treibs (1936) to make the first com- brane lipids, which are the major constitu- pelling chemical argument for the biogenic ent of extractable organic matter (bitumen) origin of petroleum. Other pigments, such in sedimentary rocks. Diagenesis quickly as carotenoids, are subject to very selective strips these compounds of their reactive preservation, generally requiring the pres- polar functionalities, and over longer peri- ence of reduced sulfur species; the functional ods causes stereochemical and structural groups that confer many of their biophysi- rearrangements, but hydrocarbon skeletons cal properties and taxonomic specificity are

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NN NN Mg Vanadyl VO Porphyrin N N N N

O O O O O

Phytane Chlorophyll a

Pristane

Z OH OH

35 35 Y OH X 29 2 2 3 3

Bacteriohopanepolyol C35 Hopane

28 29

27

28 29

27 C29 Sterane 28 29

OH 27

C29 Steroid

C29 Diasterane FIGURE 1. Structures of diagnostic phytoplankton lipids (left) and their fossil counterparts (right).

lost through chemical reduction processes of the molecular fossil record of primary early in diagenesis (e.g. Kohnen et al. 1991, producers, particularly in Paleozoic and 1993; Hebting et al. 2006). older rocks. These are the polycyclic triter- Although the preservation of pigment- penoids produced by the cyclization of the derived biomarkers is spotty and informa- isoprenoid squalene and found in the mem- tion is steadily lost over time as diagenesis branes of both and bacteria. proceeds, another class of extraordinarily The main types are the steroids, which are durable molecules provides us with much ubiquitous among the Eucarya but known

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from only a very few bacteria, and the Much of what is known about the dia- hopanoids, including the bacteriohopanep- genesis and preservation of biomarkers olyols (BHPs), produced by a wide variety derives from studies of the origin and com- of autotrophic and heterotrophic bacteria. position of petroleum (e.g., Peters et al. These molecules have the great advan- 2005). Petroleum geologists were initially tages of a durable polycyclic skeleton that interested in identifying the source rocks is clearly a biological product and a well- from which hydrocarbon accumulations characterized diagenetic fate involving a originated. Information on the thermal his- number of rearrangements that provide tories of source rocks is also key for mod- information about the postburial history of eling hydrocarbon generation. Biomarkers the organic matter. The structures of some provide a way to determine both param- commonly used biomarker lipids and their eters through complementary analyses of fossil counterparts are shown in Figure 1. sedimentary bitumen in source rocks and Table 1 summarizes current knowledge of their derived oil accumulations. Companies the biological affinities of hydrocarbons serving the petroleum exploration indus- commonly found in marine sediment sam- try have developed and maintained data- ples, excluding biomarkers derived from bases of bitumen and oil composition that terrestrial organisms. can be used to compare oils to bitumen in Molecular fossils suffer from some of their source horizons and model the ther- the same limitations as body fossils. Not all mal histories of petroleum deposits and ecologically and biogeochemically impor- that can be employed as a predictive tool tant groups leave distinctive molecular fin- when exploring in frontier regions. An gerprints, making them difficult to follow example is the commercial “Oils” database in time. Moreover, the structures of lipids generated by GeoMark Research, which are not nearly as diverse as body fossils; records geochemical analyses of more than different, often distantly related or physi- 10,000 crude oil samples from every known ologically disparate organisms can produce petroliferous basin on the globe (www.geo- similar patterns of lipids. Generally, biomar- markresearch.com). The “Oils” data com- kers will reflect an average of inputs to sedi- prise the contents of S, Ni, and V; the carbon ments, which can be influenced by factors isotopic compositions of bulk saturated and including bottom water oxygenation, sedi- aromatic hydrocarbons; and quantitative ment mineralogy, and grain surface area analysis of approximately 100 individual available for sorptive protection (Hedges hydrocarbons, including n-alkanes, acyclic and Keil 1995). These inputs are attenuated isoprenoids, steroids, and triterpenoids. by remineralization of organic matter as it Abundances of the latter biomarkers, which sinks: this reworking is >95% complete by have been determined using a rigorously 3000 m depth (Martin et al. 1987). The high reproducible analytical protocol, allow cal- degree of water-column degradation of culation of 23 diagnostic molecular ratios organic matter in deep basins means that, that can be used to predict paleoenviron- even where deep-water sediments survive mental features of an oil’s source rock subduction, they commonly contain little without direct knowledge of the rock itself organic matter; hence, the biomarker record (Zumberge 1987) or to evaluate hydrocar- of open-ocean primary production is poor. bon charge histories from field to basin The problem of interpreting absence can scales (e.g., Zumberge et al. 2005). Aver- be acute, because in biomarker analysis, aging of data from numerous oil samples absence can only be defined in terms of within a well, field, or an entire basin helps detection limits and, hence, is conditionally to overcome anomalies in individual hydro- dependent upon the analytical technology carbon samples that reflect differences in available. maturity and losses from evaporation, water

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TABLE 1. Hydrocarbon biomarkers prevalent in marine sediments and petroleum derived from marine sediments and their known source organisms

Fossil hydrocarbona Functionalized precursors Established sourcesb,c Referencesd

C27–C35 bacteriohopanes C35 bacteriohopanepolyols Bacteria although Rohmer et al. 1984, (BHPs) nonspecific 1992 2-Methylhopanes 2-Methyl-BHP although Zundel and Rohmer also in methanotrophs 1985b, 1985c; Bisseret and other bacteria et al. 1985; Summons et al. 1999 3-Methylhopanes 3-Methyl-BHP Methanotrophs, other Zundel and Rohmer proteobacteria 1985a Aryl isoprenoids, Aromatic carotenoids, e.g., Green and purple sulfur Summons and Powell isorenieratane isorenieratene, okenone bacteria 1987; Brocks et al. 2005 Gammacerane Tetrahymanol Purple nonsulfur bacteria, Ten Haven et al. 1989; some Kleemann et al. 1990 Tricyclic terpanes, Unknown Unknown, probably Moldowan and Seifert cheilanthanes bacteria 1983 [AU13]

>C20 acyclic isoprenoids Glycerol ether lipids; also Archaea although Peters et al. 2005 found as free hydrocarbons nonspecific Cholesterol and related Photosynthetic protists, Volkman 2003

C27 stero ls metazoa Ergostane; Erogosterol and related Photosynthetic protests, Volkman 2003 24-methylcholestane C28 prevalent in diatoms Stigmastane; Sitosterol, stigmasterol, Photosynthetic protests, Volkman 2003 24-ethylcholestane and related C29 sterols prevalent in chlorophytes 24-n-Propylcholestane 24-n-Propylcholesterol Marine chrysophytes Moldowan 1984 , triaromatic , dinostanol Dinoflagellates Summons et al. 1987, dinosteroids 1992; Moldowan and Talyzina 1988 24-Norcholestane 24-Norcholesterol and Diatoms Rampen et al. 2005 related 24-nor sterols

C20, C25, and C30 Mono- or polyunsaturated Diatoms Volkman et al. 1994; highly branched HBIs Belt et al. 2000; isoprenoids (HBIs) Sinninghe Damsté et al. 2004

n-C37–C39 alkenones n-C37–C39 alkenones Volkman et al. 1980; or alkanes Marlowe et al. 1984

aIn most cases, the connection between the fossil hydrocarbon and organismic source is supported by detection of diagenetic intermediates in sediments. bExtensive, systematic studies of lipids from microbial cultures are rare. Many lipid- relationships remain unknown. cGenomic sequencing will also help identify the metabolic potential of source organisms to produce preservable compounds; such identification depends on (currently incomplete) knowledge of the biosynthetic pathways of biomarker molecules. dIndicative but incomplete list. Reviews that provide extensive citation lists include Brocks and Summons 2004 and Peters et al. 2005.

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washing, or biodegradation. Although it is tion of sedimentary hydrocarbons appear to not widely appreciated, the global ubiquity be relatively invariant with age, changing of sedimentary bitumen and oil accumula- instead with source rock lithology and sedi- tions of all sizes means that hydrocarbons mentary environment. These features are can also serve as a source of information mostly reflected in the abundance patterns on trends in the global carbon cycle (e.g., of bacterial and archaeal biomarkers. An Andrusevich et al. 1998, 2000) and patterns example is depicted in Figure 2, which plots in the and environmental distri- the relative abundance of a diagnostic bac- butions of organisms, as discussed further teriohopane hydrocarbon (30-norhopane) as later. The data illustrated in Figures 2, 3, 4, a function of paleolatitude. 30-Norhopane can 5, and 6 come from the “Oils” database and arguably originate in several ways, but one represent the averages of numerous sam- particularly prolific source would be those ples from a global selection of prominent BHPs with a hydroxyl substituent at posi- Cenozoic to Proterozoic petroleum systems, tion “Z” (Figure 1); this makes them prone

both marine and lacustrine. to oxidative cleavage, leading to a C29 hydro- Inspection of trends in the “Oils” database carbon (Rohmer et al. 1992). Such precursor suggests that some aspects of the composi- BHPs occur commonly in proteobacteria,

1.8 Cenozoic Carbonate SR Mesozoic Carbonate SR 1.6 Paleozoic Carbonate SR Cenozoic Marl SR Mesozoic Marl SR 1.4 Paleozoic Marl SR Cenozoic Shale SR Mesozoic Shale SR Paleozoic Shale SR 1.2 Cenozoic Lacustrine SR Mesozoic Lacustrine SR Paleozoic Lacustrine SR 1.0 Hopane Ratio 30

/C 0.8 29 C

0.6

0.4

0.2 –80 –60 –40 –20 0 20 40 60 80 Paleolatitude FIGURE 2. This figure depicts a diagnostic biomarker ratio derived from the averaged analyses of numerous oil samples representing important commercial petroleum accumulations plotted versus their paleolatitude. Samples are grouped according to geological era and classified according to the lithology and environment of the source rock, namely marine distal shales, marine marls, marine carbonates, or lacustrine sediments. The ratio of hopanes with 29 carbons to those with 30 carbons tends to be highest in carbonates and marls and in samples from low

paleolatitude. Oils sourced from marine distal shales invariably show a C29/C30 hopane ratio <0.7, whereas marine carbonates tend to have values of 0.8 or more. This pattern holds irrespective of age over the duration of the Phan- erozoic.

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Distal Shale SR 2.0

Diatom Diversity 1.8 Genera Species 1.6

1.4 50 100

Sterane Ratio 1.2 29 Diatom Genera /C Diatom Species 28

C 1.0

0.8

0.6

0.4

0 0 0.2 0 50 100 150 200 250 300 350 400 450 500 550 600 Source Rock Age Ma FIGURE 3. The secular increase in the abundance of C28 relative to C29 steranes over the Phanerozoic Eon, par- ticularly during the last 250 million years, in petroleum systems from the GeoMark Oils database. Overlain are the fossil diatom species and genera diversity curves from Katz et al. (2004).

250 700 1.0 Cenozoic Mesozoic Paleozoic Proterozoic Carbonate SR 0.9 Marl SR

Distal Shale SR 0.8 Dinoflagellate Cyst Diversity 0.7 Genera Species 0.6

125 350 0.5

0.4 Dinoflagellate Genera Dinoflagellate Species

0.3

0.2 Relative Abundance of Triaromatic Dinosteranes

0.1

0 0 0.0 0 50 100 150 200 250 300 350 400 450 500 550 600 Source Rock Age Ma

FIGURE 4. The relative abundance of aromatic dinosteranes over the Phanerozoic Eon from the GeoMark Oils database, showing marked increase during the early Mesozoic. Note concordance with genera- and species-level dinoflagellate fossil cyst diversity curves of Katz et al. (2004). Paleozoic occurrences of dinosteranes in petroleum sources are infrequent but merit further attention.

140

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0.30 CM P Carbonate Marl 0.25 Distal Shale

0.20

0.15

0.10 2-Methylhopane Index 0.05

0.00 A 0 300 600 900 1200 1500 1800 2100 2400 2700 Age Ma

0.30 Cenozoic Mesozoic Paleozoic Precambrian

0.25 Source rocks deposited during OAEs 0.20

0.15

0.10 2-Methylhopane Index

0.05

0.00 B 0 100 200 300 400 500 600 Age Ma 0.30

Carbonate

Marl

0.25 Distal Shale

0.20

0.15

0.10 2-Methylhopane Index

0.05

0.00 C –80 –60 –40 –20 0 20 40 60 80 Paleolatitude FIGURE 5. For legend see next page (Continued)

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FIGURE 5. (Cont’d) (A) C30 2-methylhopane (2-MeHI) index (=C30 2-MeHI/(C30 2-MeHI + C30 desmethyl hopane) through geologic time. Values are generally elevated throughout the Precambrian, with distal shales reaching below 0.05 only during the Phanerozoic. Compilation includes data from the GeoMark Oils database and Kuypers et al. (2004) (B) Expansion of the time scale of (A) to focus on the Phanerozoic. Source rocks deposited during oceanic anoxic events (OAEs) are highlighted and often show elevated 2-MeHI indices. (C) 2-MeHI indices of Phanerozoic petroleum systems by source rock lithology and paleolatitude. The highest 2-MeHI values are generally found at low latitudes, often in carbonate depositional environments.

including methylotrophs. They appear to is sometimes abundant in oils from rocks be especially common in carbonate-precipi- deposited on continental margins, show- tating sedimentary environments; the ratio ing a marked increase in oils formed from

of C29/C30 hopane tends to be highest in oils Cenozoic rocks that reflects the from carbonates, intermediate in marls, and radiation of the angiosperms (Moldowan lowest in distal shales (Subroto et al. 1991). et al. 1994). Low levels of oleanane in rocks as This relationship holds independent of the old as Jurassic age, however, suggests either geological age of the source rocks. Car- that early flowering were sporadic bonates accumulate predominantly in low inhabitants of Mesozoic environments or latitudes, explaining the paleogeographic that oleanoid triterpenoid synthesis origi- correspondence shown in Figure 2. nated in their phylogenetic precursors (e.g., In contrast to the trends shown by Peters et al. 2005). Observations concerning biomarkers from , acyclic and algal biomarkers are discussed later. cyclized terpenoids and steroids (Figure 1) derived from planktonic algae and vascular II. THE RISE OF MODERN plants show strong age-related trends (e.g., PHYTOPLANKTON Summons and Walter 1990; Brocks and Summons 2004). For example, the oleanoid A. Fossils and Phylogeny triterpenoids such as β-amyrin are impor- tant in the predation-defense mechanisms In modern oceans, three algal groups of flowering plants. Oleanane, a hydro- dominate primary production on continen- carbon derived from these triterpenoids, tal shelves: the diatoms, dinoflagellates, and

B D E

A C F

FIGURE 6. Proterozoic and Early protistan microfossils. (A) and (B) are Neoproterozoic leiospherid acri- tarchs; (C–F) are Early Cambrian acritarchs (C–E) and a prasinophyte phycoma (F; Tasmanites). Scale bar = 40 microns.

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coccolithophorids. As detailed elsewhere ular clocks date divergence within a closely in this volume, fossils clearly suggest that related group of unicellular that these groups all rose to taxonomic and eco- subsequently and individually were incor- logical prominence only during the Meso- porated as plastids in chromalveolate algae, zoic Era (Delwiche, 2006; de Vargas et al. or photosynthetic chromalveolates emerged 2006; Kooistra et al. 2006). Could there have from a single Proterozoic endosymbiosis been, however, an earlier “cryptic” evolu- (Cavalier-Smith 1999) but remained ecologi- tionary history for these groups? For exam- cally unimportant or paleontologically unrec- ple, might nonmineralizing stem group ognizable until much later. diatoms or haptophytes have been ecologi- cally important but paleontologically unin- B. Biomarkers and the Rise of terpretable in Paleozoic oceans? Might the Modern Phytoplankton significance of Paleozoic dinoflagellates be obscured by fossils that are abundant and The rise to ecological prominence of the diverse but lack archeopyles? three chlorophyll c-containing eukaryotic Several reports claim evidence plankton lineages left several imprints in for Paleozoic diatoms, dinoflagellates, and the molecular fossil record, especially in the haptophytes, but such fossils are rare and distributions of steranes with different side- subject to alternative interpretation as con- chain alkylation patterns. A secular increase taminants (the mineralized skeletons) or in the ratio of C28 to C29 steranes (24-methylc- different taxa (organic fossils). Stratigraphic holestanes versus 24-ethylcholestanes), first research indicates that the Paleozoic silica noted by Grantham and Wakefield (1988), cycle differed substantially from that of has been attributed to increasing production the Cretaceous and Tertiary periods, with by chlorophyll c algae (which dominate C28 and radiolarians dominating biolog- sterane input) relative to , which ical removal of silica from the oceans (Maliva synthesize primarily C29 steroids (Volkman et al. 1989). Similarly, sediments preserved in 2003). An updated plot of the C28/C29 ster- obducted slices of Paleozoic seafloor at best ane ratio versus geological age, and based contain only limited evidence for pelagic car- on averages from 123 petroleum systems bonate deposition. Such observations cannot worldwide, is shown in Figure 3 along with eliminate the possibility that rare diatoms, data for diatom diversity. The C28/C29 ster- coccolithophorids, or calcareous dinoflag- ane ratio remains below 0.4 in the Neopro- ellates lived in Paleozoic oceans, but they terozoic and, with one exception, below 0.7 clearly indicate that these groups did not through the Paleozoic. Corresponding to perform the biogeochemical roles they have the diversification of diatoms in the later played since the Mesozoic Era. half of the Mesozoic, there is a rise in the Complementing this, C28/C29 sterane ratio to values as high as estimates for diatom and coccolithophorid 1.8, followed by an apparent drop in the diversification, calibrated by well-preserved and . Values climb again fossils, suggest that these groups have no in the , accompanying a second rise long Paleozoic “prehistory” (de Vargas in the numbers of diatom genera and spe- et al. 2006; Kooistra et al. 2006). On the other cies. hand, some molecular clock analyses sug- Other biomarkers show marked increases gest divergence times for the plastids in in abundance in the Cretaceous that also photosynthetic chromoalveolates well back likely reflect diatom radiation. These include into the Proterozoic (Douzery et al. 2004; 24-norcholestanes (Holba et al. 1998a, b), Yoon et al. 2004). If these estimates are even the so-called highly branched isoprenoids broadly correct, they must be accommo- (HBIs; Sinninghe Damsté et al. 1999a, b; Belt dated in one of two ways. Either the molec- et al. 2000; Allard et al. 2001), long-chain

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diols, and mid-chain hydroxyl methy- 24-norcholesta-5,22-dien-3β-ol by Rampen lalkanoates (Sinninghe Damsté et al. 2003). et al. (2005) in a cold water diatom species, The secular increase in 24-norcholestane provide a timely reminder that biomarkers abundance (Moldowan et al. 1991; Holba not only reflect the presence of particular et al. 1998a, 1998b) was observed and linked algal taxa but also reflect the environmental to the diatom radiation well before a pre- conditions under which they thrive. A corol- cursor was recognized in a culture of lary to this is that cultured organisms might the centric diatom Thalassiosira aff. antarctica not always produce the same assemblage of (Rampen et al. 2005). In fact, in the study lipids as their counterparts growing under of Rampen et al. (2005) only one, that is natural conditions. T. aff. antarctica, of 100 different diatom taxa The other major class of diatom-specific was found to produce 24-norcholesta-5, biomarkers is the HBI. So far as is currently 22-dien-3β-ol . known, the occurrence of HBI is confined The detail of novel sterol production by to four genera, namely , Haslea, diatoms provides an interesting window and Pleurosigma within the pennates and into the connections among biomarkers, Rhizosolenia among the centrics (Volkman , and the physiological roles of et al. 1994; Belt et al. 2000; Sinninghe Damsté lipids. In a recent study of diatom sterols, et al. 2004). Both molecular phylogeny and Suzuki et al. (2005) reported that environ- fossils indicate that ce ntric diatoms pre- mental samples of diatoms collected from date pennates (Kooistra et al. 2006). There- the North Pacific Ocean and the Bering Sea fore, the genus Rhizosolenia is considered contained 24-norsterols. Further, samples the likely source of the first recorded fossil of the diatom Coscinodiscus marginatus, ini- HBI at about 91 Ma ago—which predates tially devoid of 24-norcholesterol, contained recorded fossil tests of Rhizosolenid dia- significant amounts of this and the related toms by about 20 million years (Sinninghe steroid 27-nor-24-methylcholesta-5,22-dien- Damsté et al. 2004). This discrepancy in tim- 3β-ol after storage at 3°C for 30 days. These ing could reflect incomplete paleontological authors attributed the latter change to bac- sampling, which systematically underes- terial biodegradation. Due to the ubiquity timates first appearances, HBI synthesis of 24-norsteranes in Mesozoic sediments by a morphologically distinct stem group (Holba et al. 1998a, 1998b), and no other relative of the rhizosolenids, or both. Bio- evidence for selective side-chain biodegra- synthetic pathways are such a fundamental dation of sterols (biodegrading bacteria are characteristic of organisms that they might

unlikely to select for removal of C26 and C27 of be detectable through chemical fossils the apparent precursor 24-methylcholesta- before the first classical fossils of a are 5,22-dien-3β-ol and leave other sterols un- ever recognizable. touched), it seems far more likely that there Dinosteroid biomarkers, derived from the is a direct as opposed to diagenetic source 4-methylsterols of dinoflagellates (Robinson for the 24-norsteroids in sediments. The et al. 1984), show an analogous pattern of rarity of 24-norsterols in cultured diatoms secular increase in the Mesozoic, in accord (Rampen et al. 2005) more likely reflects with microfossil evidence for later Trias- the fact that sterol biosynthesis responds to sic dinoflagellate radiation. As in the case physiological conditions and that laboratory of diatom HBI, however, several reported culture conditions have as yet not mimicked occurrences of dinosteranes predate fossil the natural conditions, such as low tempera- cysts, in some cases by hundreds of millions ture and, perhaps, low light under which 24- of years (Summons et al. 1992; Moldowan norsterols are produced by some diatoms. and Talyzina 1998; Talyzina et al. 2000). The enigma surrounding the origins of 24- These deserve close attention as they may norsteroids, and the ultimate detection of establish a genuine pre-Mesozoic history

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of dinoflagellates, as predicted by molecu- 2-MeHI values are found in oils from car- lar phylogenies and clocks. Some aspects bonate lithologies, formed predominantly of this putative history are considered fur- at low paleolatitudes [Figure 5C].) The ther later. In Figure 4, data derived from the exceptions are associated with widespread “Oils” database show the pattern of secular anoxia in the oceans (Figure 5B). Kuypers variation in triaromatic dinosteroid abun- et al. (2004a, 2004b) and Dumitrescu and dances, along with a recent compilation Brassell (2005) studied biomarkers associ- of dinoflagellate cyst diversity (Katz et al. ated with Cretaceous oceanic anoxic events 2004). (OAEs) and found that the relative abun- The third group of modern plankton, the dances of 2-methylhopanoids, as measured haptophytes, produces distinctive lipids in by the 2-MeHI, were distinctively enhanced,

the form of long-chain (n-C37 to C39), unsatu- along with nitrogen (N) isotopic evidence rated ketones known as alkenones (Volkman for cyanobacterial primary productivity et al. 1980; Marlowe et al. 1984). These can be (Kuypers et al. 2004b). Mass at abundant and easily recognized in Recent the - boundary is also asso- and Cenozoic sediments that have not expe- ciated with widespread anoxia in shallow rienced extensive diagenesis, and they form oceans (Wignall and Twitchett 2002). In the basis of a widely used paleotempera- Figure 5, the two data points for the Per- ture proxy (Brassell et al. 1986). Their dis- mian Triassic transition represent unpub- tinctiveness, however, lies in the carbonyl lished data from the Perth Basin, , functionality and one to four unsaturations, and the boundary stratotype in Meishan, which are easily reduced and inherently China; in these sections high 2-MeHI cor- unstable over geological time scales (Prahl relate with independent molecular, iron et al. 1989). Thus, the oldest reported detec- speciation, and sulfur isotopic evidence tion is in Cretaceous sediments (Farrimond for intense euxinia (Grice et al. 2005). The et al. 1986), and we would not expect to be highest 2-MeHI value (0.29) recorded in able to recognize them in Paleozoic or older the GeoMark Oils database comes from the rocks. Larapintine Petroleum System, Australia, The molecular and morphological which includes oils from the Late Devo- records of eukaryotic predominance in shelf nian complex of the Canning Basin primary production are mirrored by indica- (Edwards et al. 1997) sourced from black tions of relatively low cyanobacterial contri- shales deposited near to Frasnian-Famen- butions. Some cyanobacteria are known to nian boundary, another event characterized biosynthesize BHPs and analogues with an by geological and geochemical evidence for extra methyl group attached to the 2 posi- pervasive euxinia (e.g., Bond et al. 2004). tion of the A ring (2-MeBHP); the hydro- The samples from the Cretaceous OAEs, carbon cores of these molecules provide a Permian-Triassic boundary, and Frasnian- potentially useful tracer for cyanobacterial Fammenian shale all contain abundant iso- input to sedimentary organic matter (Sum- renieratane and aryl isoprenoids derived mons et al. 1999). Apart from a few notable from the brown pigmented strains of the exceptions, values of the 2-methylhopane green sulfur bacteria (Chlorobiaceae), con- (2-MeHI) index fraction of hopanoids sidered diagnostic for photic zone euxinia methylated at the 2 position relative to their (e.g., Summons and Powell 1987; Koop- desmethyl counterparts) tend higher in Pro- mans et al. 1996; Kuypers et al. 2004a; Grice terozoic samples than they are in Paleozoic et al. 2005; van Breugel et al. 2005). Kuypers and, especially Jurassic and younger oils et al. (2004b) hypothesize that the N cycle (Figure 5A). This is especially true of sam- was compromised while euxinic conditions ples from shales. (Examination of the Phan- prevailed during the Cretaceous OAEs, erozoic record [Figure 5B] shows that higher creating an unusual opportunity for the

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proliferation of N-fixing cyanobacteria. The resemble dinocysts, but lack archeopyles. disparate occurrences described previously Still other acritarchs (the group name given suggest a more general correlation between to closed, organic-walled microfossils of high 2-MeHI and photic zone euxinia, a uncertain systematic relationships) (Evitt topic we return to in our discussion of Prot- 1963) do not closely resemble known cysts erozoic primary production. of modern phytoplankton. Collectively, Although cyanobacteria appear to have these microfossils show evidence of marked been minor contributors to primary produc- Cambrian and radiations that tion on most Mesozoic and Cenozoic conti- parallel the two-stage diversification of nental shelves, they remain the dominant marine (Knoll 1989). For reasons phytoplankton in open-ocean, oligotrophic that remain obscure, diversity environments today. Whether this is a drops near the end of the and recent or long-standing situation is difficult remains low for the remainder of the Paleo- to discern given the paucity of the deep- zoic Era (Molyneux et al. 1996). sea sedimentary records and the absence of Moldowan and Talyzina (1998) innova- 2Me-BHP in cyanobacterial picoplankton tively attempted to break the phylogenetic (Summons, unpublished data). impasse regarding Cambrian microfos- sils. Extracts from fossiliferous clays of the C. Summary of the Rise of Modern Lower Cambrian Lükati Formation, Esto- Phytoplankton nia, contain low abundances of dinoster- ane and 4a-methyl-24-ethylcholestane, both Fossils, molecular biomarkers, molecular known to originate from the sterols of clocks for individual clades, and the sedi- dinoflagellates (Robinson et al. 1984; Sum- mentary silica record all tell a consistent mons et al. 1987). Moldowan and Talyzina story: the modern phytoplankton has Mes- (1998) divided the microfossil populations ozoic roots. How we interpret this transfor- in a Lükati sample into three groups—tas- mation depends in no small part on what manitids (Figure 6F; interpreted as prasi- we think came before. nophyte phycomata), a low fluorescence group dominated by leiosphaerid acritarchs III. PALEOZOIC PRIMARY (also possible phycomata of prasinophytes PRODUCTION like the extant Halosphaera), and a high fluorescence fraction containing abundant A. Microfossils process-bearing acrtiarchs (e.g., Figure 6D)— and analyzed the sterane content of these Microfossils of presumptive eukaryo- subassemblages. The tasmanitid and low tic phytoplankton are both abundant and fluorescence fractions contained relatively diverse in Paleozoic marine rocks (Figure abundant C steranes but little or no dino- Tas- 29 6C–F). A number of forms, including lipid. In contrast, the high fluo- manites, Pterospermella, Cymatiosphaera, and rescence fraction contained relatively high have morphologies and ultrastructures that abundances of dinosterane, suggesting that relate them to prasinophyte phycomata the dominant, process-bearing acritarchs are (Tappan 1980). Indeed, in well-studied dinocysts sans archeopyles. It is not clear that microfossil assemblages from Lower Cam- sterols play a structural role in cyst walls, brian shales, at least 20% of described making selective adsorption a real possi- morphotaxa and more than half of all indi- bility. Moreover, whereas dinosterane and vidual fossils are likely prasinophytes (e.g., 4a-methyl-24-ethylcholestane abundances et al Volkova . 1983; Knoll and Swett 1987; in these samples are relatively high, their Moczydlowska 1991). Others, with regu- concentrations are absolutely low. Thus, larly distributed processes, tantalizingly the specific attribution of acritarch taxa to

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the dinoflagellates remains speculative. C28 homologues suggests a greater role for Nonetheless, these analyses do clearly sug- green algae in marine primary production gest that dinoflagellates were present in at this time. This signal is observed in glo- coastal Cambrian oceans and may have left bally distributed rocks and petroleum sys- a morphological as well as biogeochemical tems from the latest Neoproterozoic into the record. Given the low abundances of dino- Paleozoic and wanes in the later Paleozoic, flagellate biomarkers, it is possible that the although the depositional bias for much constituent dinoflagellates were largely het- of this time is toward low paleolatitudes erotrophs, not primary producers. (Figure 7). In a study of tasmanite oil shales from different locations in Tasmania, Revill et al. (1994) found that C and C steranes B. Paleozoic Molecular Biomarkers 27 29 were present in roughly equal abundance

The molecular fossil record prior to the and dominated over C28. All the samples rise of the chlorophyll c lineages broadly were shales with a high total organic car- corroborates the microfossil evidence for bon content, with the visible organic matter the occurrence and potential ecological primarily comprising Tasmanites punctatus importance of other eukaryotic phytoplank- microfossils. These early Permian deposits, ton in the Paleozoic. In particular, the high which were geographically localized, con-

abundance of C29 steranes relative to C27 and tained abundant dropstones and evidence

C29 Zhetebay C29 C29 Kazakhstan C28 South Chona Siberia C27 Rodda Beds Australia

C28 C C 27 27 C28

Laurentia

C C29 Gondwana 29

Marmul Baghewala Oman India

C C27 C28 27 C28

FIGURE 7. Dominance of C29 steranes in late Neoproterozoic/Early Cambrian petroleum systems. Paleogeogra- phy shows concentration of depositional systems to low paleolatitudes during this time. Continental reconstruc- tion redrawn after C. Scotese, available at www.scotese.com.

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of low temperature minerals, were clearly fossils, predominantly of calcareous skel- glacial in origin. Thus, the Tasmanites punc- etons, further indicate that red and green tatus may have occupied an ecological niche algae were ecologically important in the similar to that occupied by modern sea-ice shallow shelf benthos (Wray 1977). diatom communities (Revill et al. 1994). Dinosteranes are generally below detec- tion in the Paleozoic marine sediments and IV. PROTEROZOIC PRIMARY oils that have been examined and reported PRODUCTION to date. In contrast, triaromatic dinosteroids have been found in significant abundance Fossils (whether morphological or molec- in several lower Paleozoic sedimentary ular) are less abundant in Proterozoic rocks rocks and petroleum samples. This speaks than they are in Phanerozoic samples, and to the occurrence of either stem or crown Proterozoic sedimentary rocks, themselves, group dinoflagellates in Paleozoic oceans. are less abundantly preserved than their An additional factor in observed dinoster- younger counterparts. Nonetheless, fossils ane abundances may be preservational bias. have been reported from hundreds of Pro- Saturated dinosteroids, dinosteranes, may terozoic localities (Mendelson and Schopf only be preserved under strongly reducing 1992), allowing us to recognize at least broad conditions. A wider search for triaromatic patterns of stratigraphic and paleoenviron- dinosteroids, and authentication of the mental distribution. Indeed, Proterozoic Paleozoic petroleum data through reanaly- micropaleontology has developed to the sis and careful checking of pedigrees, may point where it has become predictive, in the expose a more extensive pattern of occur- sense that knowledge of age and environ- rence and, hence a richer early history for mental setting permits reasonable predic- these plankton than is evident from the tion about the fossil content of a given rock distribution of fossilized cysts. sample (e.g., Knoll et al. 2006).

C. Paleozoic Summary A. Prokaryotic Fossils Biomarker data for oils and some sedi- By the earliest Proterozoic Eon, cyano- ments suggest that dinoflagellates existed bacteria must have been important contrib- in Paleozoic oceans, but with few excep- utors to primary production—there is no

tions, lipids thought to be sourced by dino- other plausible source for the O2 that began occur in low abundances, raising to accumulate in the atmosphere and sur- the question whether Paleozoic dinoflag- face oceans 2.45–2.32 Ga. Consistent with ellates functioned to any great extent as this observation, it has been appreciated primary producers. The same is true of since the early days of Precambrian paleon- possible stem-group . Thus, tology that cyanobacteria-like microfossils although Chl a+c phytoplankton may well are abundant and widespread constituents have existed in Paleozoic oceans, they do of Proterozoic fossil assemblages (Figure 8; not appear to have played anything like the Schopf 1968). Not all cyanobacteria have ecological role they have assumed since the diagnostic morphologies, but some do and Mesozoic Era began. In contrast, microfossil others are likely candidates for attribution and biomarker molecules both suggest that given knowledge of taphonomy (processes green algae played a greater role in marine of preservation) and depositional environ- primary production than they have in the ments represented in the record. By mid- past 100 million years, and biomarkers also Proterozoic times, if not earlier, all major suggest a significant role for cyanobacterial clades of cyanobacteria existed in marine production on continental shelves. Macro- and near-shore terrestrial environments,

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A B

C D

FIGURE 8. Cyanobacteria in Proterozoic sedimentary rocks. (A) 700–800 million-year-old endolithic pleur- capsalean fossil. (B) 1500 million-year-old mat building cyanobacterium closely related to modern Entophysalis. (C) 1500 million-year-old short richome. (D) Spirulina-like fossil in latest Proterozoic (<600 Ma) phosphorite. Scale bar = 15 microns in (A–C), and = 25 microns in (D).

including those that differentiate akinetes on a calibrated by well- and heterocysts (Tomitani et al. 2006). The documented fossils, however, it is likely that best characterized Proterozoic cyanobacte- cyanobacteria were important constituents ria come from early diagenetic nod- of the phytoplankton in Proterozoic oceans ules in carbonate successions (e.g., Schopf (Sanchez-Baracaldo et al. 2005; Tomitani et al. 1968; Zhang 1981; Knoll et al. 1991; Sergeev 2006; see later). et al. 1995, 2002; Golubic and Seong-Joo 1999). These fossils are largely benthic and B. Eukaryotic Fossils largely coastal marine. Stromatolites, how- ever, indicate a much wider distribution of Two problems shadow attempts to under- benthic cyanobacteria in the photic zone. stand the Proterozoic history of photosyn- (A role for cyanobacteria or of organisms thetic eukaryotes. Given the polyphyletic in general is difficult to establish in the pre- evolution of at least simple unicellular and cipitated stromatolites found in Earth’s old- multicellular characters, convergence com- est well preserved sedimentary successions; plicates interpretation of many Proterozoic however, the likelihood that cyanobacteria protistan fossils. In addition, given the oft- were major architects of Proterozoic stroma- observed reality that stem group organisms tolites that accreted primarily by trapping display only a subset of the characters that and binding is high) (Grotzinger and Knoll collectively identify crown group members 1999). Microfossils are less useful for evalu- of clades, early fossils may challenge finer ating the contributions of cyanobacteria to scale systematic attribution, even though the phytoplankton of Proterozoic oceans they may be unambiguously eukaryotic. because many were small, nondescript, and Despite these problems, a small number likely to settle on the seafloor in places where of fossil populations provide calibration interpretable preservation was improbable. points for eukaryotic phylogenies. Bangi- Given the distribution of planktonic clades omorpha pubescens (Butterfield 2000) is a large

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population of multicellular microfossils sedimentary rocks. As noted previously, found in tidal flat deposits of the ca. 1200 Ma the three major types of ornamented phy- Hunting Formation, Arctic . These coma known from living prasinophytes erect filaments, preserved via rapid burial have fossil records that extend backward to by carbonate mud and subsequent silicifi- the Early Cambrian, but there is little evi- cation, display patterns of thallus organiza- dence of earlier origin. In contrast, extant tion, cell division, and cell differentiation Halosphaera develop smoothly spheroidal that ally them to the bangiophyte red algae. phycomata that could easily be represented Complementing this, a moderate diversity among leiosphaerid acritarchs in Protero- of cellularly preserved florideophyte red zoic rocks (Figure 6A and B; Tappan, 1980). algal thalli occurs in <600 Ma phosphorites Ultrastructural and microchemical studies of the Doushantuo Formation, (e.g., Javaux et al. 2004; Marshall et al. 2005) China (Xiao et al. 2004). Shifting to another provide our best opportunity to test this branch of the eukaryotic tree, several taxa hypothesis. of vase shaped microfossils in the ca. 750 Chromalveolates may be recorded Kwagunt Formation, Grand Canyon, Ari- in a very different way. In 1986, Allison zona, can be related to lobose testate amoe- and Hilgert reported small (7–40 µm in bae, placing a minimum constraint on the maximum dimension), apparently siliceous timing of amoebozoan divergence (Porter et ovoid scales in of the Tindir Group, al. 2003). northwestern Canada, now judged to be Accepting the presence of red algae by >635 and <710 Ma (Kaufman et al. 1992). 1200 Ma, one might expect to observe green The scales resemble those formed by liv- algal fossils in younger Proterozoic rocks. ing prymnesiophytes and (at a smaller size Several candidate taxa have been described, range) chrysophytes, likely documenting of which Proterocladus, a branching coeno- early diversification somewhere within the cytic thallus organized much like living chromalveolate branch of the eukaryotic Cladophora, is most compelling (Butterfield tree. et al. 1994). Palaeovaucheria clavata, described Fossils of any kind are rare in rocks from >1005 ±4 Ma shales in Siberia (Herman older than about 2000 million years, but 1990), as well as ca. 750–800 Ma shales from unambiguous fossils of eukaryotes occur Spitsbergen (Butterfield 2004), has a branch- in shales as old as 1650–1850 Ma (Knoll ing filamentous morphology and pattern of et al. 2006); little is known about their reproductive cell differentiation very simi- systematic relationships or physiology. lar to that of the extant xanthophyte alga Compilations of total diversity (e.g., Knoll Vaucheria. Kooistra et al. (2006) speculate 1994; Vidal and Moczydlowska 1997), that this similarity arose via convergence assemblage diversity (Knoll et al. 2006), in a green algal clade; either interpretation and morphospace occupation (Huntley places the origin of green algae earlier than et al. 2006) through time agree that a mod- 1000 Ma. erate diversity of eukaryotic organisms Fossils show that eukaryotic photoau- existed in oceans. By totrophs were present in the benthos no ca. 1200 Ma if not earlier, this diversity later than the Mesoproterozoic Era (1600– included photosynthetic eukaryotes. Diver- 1000 Ma), but what about the phytoplank- sity appears to have increased modestly in ton? Unicellular taxa occur in all three the Neoproterozoic, but the major radia- divisions of the Plantae, making it likely tions within preservable and that such cells existed by the time that Ban- phytoplankton groups took place only at giomorpha evolved. Of these, however, only the end of the Proterozoic Era and dur- the phycomate prasinophytes are likely to ing the ensuing Cambrian and Ordovician have left a tractable fossil record in marine Periods (Knoll et al. 2006).

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C. Proterozoic Molecular Biomarkers Australia contain rocks of low to moderate thermal maturity, more consistent with the Rocks containing organic matter amena- probability of finding genuinely syngenetic ble to biomarker analysis grow increasingly biomarkers. Given that studies of the Roper rare as we sample more deeply into the Pro- and McArthur Basin sediments and oils terozoic, and many of those available have consistently show the presence of steroids undergone extensive heating such that only (Summons et al. 1988a, 1988b; Dutkiewicz the most recalcitrant molecules remain. et al. 2003) along with other evidence for the Nevertheless, a molecular fossil record of in situ (Summons et al. 1994) character of primary production is emerging for this long the bitumens, there seems little doubt that interval of Earth history. A major feature of steroid biosynthesis operated as long ago as the record is the high relative abundance 1640 Ma. Preservation is a major limitation of 2-MeHI in organic-rich distal shales for both body and molecular fossil records throughout the Proterozoic (Figure 5), which, at this point. Nonetheless, sterane abun- in conjunction with the microfossil record dances in rocks of this age appear to be low and geochemical evidence for oxic sur- independent of maturity level and do not face waters in oceans, provides strong evi- approach Phanerozoic abundances until the dence for the importance of cyanobacterial Neoproterozoic Era. Based on a few excep- production. There has been such limited tionally well-preserved deposits of organic sampling of Paleo- and Mesoproterozoic material in Mesoproterozoic shales, there sediments that it has not been possible to appear to have been times and places where examine these for correlations with lithology, producer communities were very different as has been accomplished for the Phanerozoic from those that characterize later periods. (Figure 5C). Brocks et al. (2005) have reported biomarkers Steranes have been reported from a num- of anaerobic, sulfide-utilizing phototrophs ber of Proterozoic successions (e.g., Summons in the carbonate facies of the Barney Creek and Walter 1990; Hayes et al. 1992; Dutkie- Formation, Australia, suggesting that eux- wicz et al. 2003) and are generally found in inic waters extended well into the photic low abundance, reflecting at least in part the zone. Molecular markers of eukaryotes thermal maturity of their host rocks. These and cyanobacteria in those portions of the molecular fossils establish the presence of Barney Creek Formation are exceptionally eukaryotes in Proterozoic oceans, but the scarce, raising the possibility that, in at least scarcity of detailed records limits the infer- some environments during the Proterozoic, ences that can be drawn concerning eco- production by anoxygenic photoautotrophs logical role or taxonomic affinities (because may have been quantitatively important. group-distinctive markers are generally In fact, the scarcity of steroids and 2- below detection limits). The geologic record methylhopanoids in samples with most of steroid biosynthesis extends into the Late abundant biomarkers for phototrophic sul- Archean, several hundred million years fur bacteria is also consistent with the highly before the first recognized protistan fossils. euxinic conditions they require. The extent However, there continue to be doubts about to which this scenario reflects global versus the syngeneity of these steroids because of local conditions awaits further elucidation, the advanced maturity of all the sections but it is consistent with geochemical prox- studied so far and because of the poten- ies for oceanic redox conditions, observed tial for the bitumens found there to have globally (e.g., Logan et al. 1995; Arnold et al. migrated from younger sequences or to be 2003; Shen et al. 2003; Gellatly and Lyons contaminants from drill and handling (e.g., 2005). Brocks et al. 2003a, 2003b). In contrast, the In contrast to the scarcity of suitable Roper and McArthur Basins of northern organic-rich rocks in the Paleoproterozoic

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and Mesoproterozoic successions, the Neo- tic algae contributed to primary production proterozoic is replete with well-character- during at least the last 600 million years of ized organic matter in low maturity sections the Proterozoic Era. Yet, preserved biomar- from Australia, North America, Oman (e.g., kers are dominated by cyanobacteria and Grantham et al. 1987) and eastern Siberia other photosynthetic bacteria, suggesting (Summons and Powell 1992; see Summons that eukaryotes played a limited quantita- and Walter 1990 and Hayes et al. 1992, for tive role in primary production. Increas-

reviews). Of particular note are the oldest ing amounts of C29 steranes appear in later commercial petroleum accumulations in Neoproterozoic samples, typified by the Siberia and Oman. These late Neoprotero- high sterane to hopane ratios and strong

zoic oils display striking biomarker patterns C29 sterane predominances in oils from the characterized by particularly abundant South Oman Salt Basin and eastern Siberia steroidal hydrocarbons. Predominance of (e.g., Grantham 1986; Summons and Powell

C29 steranes over other homologues is a fea- 1992); this suggests that green algae began ture of oils from the South Oman Salt Basin to play an increasing role in primary pro- that has received much attention since it duction by 600–700 Ma. The timing of this was first reported by Grantham (1986). transition is not well constrained but, in Examination of Neoproterozoic petroleum Oman, it begins prior to the Marinoan samples worldwide suggests that this is a glaciation and extends to the Neoprotero- globally significant feature (Figure 7) that zoic-Cambrian boundary (Grosjean et al. records the rise of green algae to ecologi- 2005, and unpublished data), falsifying the cal prominence. Further, samples that show hypothesis that the green algal prolifera-

the strong predominance of C29 steranes tion was a response to the Acraman impact are also generally characterized by anoma- event in Australia (McKirdy et al. 2006). In lously light carbon isotopic compositions, short, algae may have emerged as major [AU1] in the range of −33 to −37% PDB. It is likely contributors to global primary production no coincidence that the oldest commercial only during the late Neoproterozoic to Early petroleum deposits bear the prominent Paleozoic interval distinguished by marked signature of a green algal contribution to increases in fossil diversity. petroleum-prone organic matter and that some green algae are known for their capac- ity to biosynthesize decay resistant aliphatic V. ARCHEAN OCEANS biopolymers in their cell wall (algaenans; Derenne et al. 1991, 1992; Gelin et al. 1996, We evaluate the Archean geobiologi- 1997, 1999), a likely source of acyclic hydro- cal record cautiously, as available data are carbons in these oils (e.g. Höld et al. 1999). sparse. Sedimentary rocks are limited in volume, especially for the early Archean, and most surviving strata have been altered D. Summary of the Proterozoic Record by at least moderate metamorphism. Thus, Microfossil and biomarker records are any interpretation must be provisional. consistent in showing that cyanobacteria The expectation from both phylogeny and and eukaryotic microorganisms were both the Proterozoic biogeochemical record is that present in Proterozoic oceans. Fossils indi- prokaryotic primary producers are likely cate that the primary endosymbiotic event to have governed early marine ecosystems. establishing the photosynthetic Plantae took Cyanobacteria have the ecological advantage place no later than ca. 1200 Ma, in broad of obtaining electrons from ubiquitous agreement with molecular clock estimates water molecules, but there is no reason to appropriately ornamented by error esti- believe that cyanobacteria were the primor- [AU2] mates (Hackett et al. 2006). Thus, eukaryo- dial photoautotrophs (see Blankenship et al.

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2006). Indeed, the question of when cyano- genicity is harder to establish. Conoidal bacteria, with their coupled photosystems, forms in ca. 3450 Ma rocks from Western evolved remains contentious. In an early Australia (Hofman et al. 1999; Allwood et al. ocean dominated by anoxygenic photo- 2006) and “roll-up structures” (sediment bacteria, the availability of electron donors sheets that were ripped up and rolled into ++ (Fe , H2, H2S) would have limited primary a cylinder by currents, suggesting microbi- production (Kharecha et al. 2005). ally mediated cohesion of poorly lithified The four principal lines of evidence used laminae) in comparably old rocks from to contract an evolutionary history of Prot- South Africa (Tice and Lowe 2004) may well erozoic oceans apply equally to the Archean require biological participation to form, but record: microfossils, biomarker molecules, the taxonomic and physiological nature of sedimentary textures that record microbe/ the participants remains uncertain (see Tice sediment interactions on the ancient sea- and Lowe 2006, for an argument that anox- floor (e.g., stromatolites), and stable isotopic ygenic photobacteria fueled Early Archean signatures (Knoll 2003b). Few microfossils mat ecosystems). have been reported from Archean cherts No biogeochemically informative organic and shales. Somewhat poorly preserved molecules are known from Early Archean fossils occur in latest Archean cherts from rocks. Late Archean biomarkers have been South Africa (Lanier 1986; Klein et al. 1987; reported; controversy surrounding their Altermann and Schopf 1995); these could identification and interpretation has two dis- include cyanobacteria, but other alterna- tinct aspects. The first relates to their prov- tives cannot be rejected. More controversial enance and whether or not all the organic are the nearly 3500 Ma carbonaceous micro- matter present in ancient sediments is coe- structures interpreted as bacterial, and pos- val, as recognized by Brocks et al. (2003a, sibly cyanobacterial trichomes by Schopf 2003b). This question can best be addressed (1993). Recently, not only their systematic through studies of cores recently drilled and interpretation but their fundamental inter- curated under controlled conditions. For pretation as biogenic has been called into example, the Agouron-Griqualand Paleo- question (Brasier et al. 2002, 2005, 2006). proterozoic Drilling Project (AGPDP) and Debate about these structures continues the NASA Institute Drilling (e.g., Schopf et al. 2002a, 2002b, in response Project (ABDP) have recovered fresh cores to Brasier et al. 2002), but few believe that from South Africa and the Craton of these structures, whatever their origin, pro- , respectively, which are vide phylogenetic or physiological insights being studied for a range of paleobiologic into early life. proxies, including analyses of preserved The stromatolite record is similar. At organic matter. One aim of this research is least 40 occurrences of stromatolites have to control or eliminate contamination by been reported from Archean rocks (Schopf hydrocarbons from younger sediments; 2006)—not a lot given that the record is a second aim is to test for relationships 1 billion years long. Those younger than between extractable hydrocarbons and rock about 3000 Ma include structures that accreted properties that could not exist in the case of by the trapping and binding of fine parti- contamination. cles; such textures are more or less uni- The second aspect of the controversy formly associated with microbial activity. revolves around the degree to which bio- Bedding surfaces on siliciclastic rocks of synthetic pathways may have evolved over comparable age similarly include textures long time scales. It is fair to state that there attributable to communities must have been evolution in the structure (Noffke et al. 2006). Older stromatolites are and function of lipids over geological time. largely precipitated structures whose bio- However, key enzymes in the biosynthetic

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pathways leading to sterols (Summons to nearly 3800 Ma metamorphosed sediments et al. 2006) and other triterpenoids in extant from southwestern Greenland (Rosing and organisms are highly conserved. The known Frei 2004). The question is whether these sig- geological record of molecular fossils, espe- natures require such an interpretation. Other cially steranes and triterpanes, is notable biochemical pathways for carbon fixation for the limited number of structural motifs exist and at least some of them impart iso- that are recorded. With a few exceptions, topic signatures that are equally consistent the carbon skeletons are the same as those with Archean data (e.g., Knoll and Canfield found in the lipids of extant organisms, and 1998). It has been known for 2 decades that no demonstrably extinct structures have abiotic syntheses of organic matter, like that been reported. Furthermore, the patterns of demonstrated by Miller (1953), fractionate occurrence sterane and triterpane isomers C-isotopes (Chang et al. 1982); the degree are rigid over billion-year time scales and of fractionation appears to vary widely as a correlate strongly with environments of function of initial conditions. More recently, deposition, suggesting that diagenetic path- McCollom and Seewald (2006) have shown ways connecting functional lipids to their that Fischer-Tropsch-type (FTT) synthesis fossil biomarker counterparts are also con- can produce organic compounds depleted served. We also have evidence, through the in 13C relative to their carbon source to a occurrence of rearranged steranes (diaster- degree similar to that associated with bio- anes) and unconventional steroids such as logical carbon fixation. In these experi- the 2-alkyl and 3-alkyl steranes (Summons ments, formic acid was reacted with native and Capon 1988, 1991) and their aromatic iron at 250°C and 325 bar, and a series of counterparts (Dahl et al. 1995), that fossil n-alkanes were produced that were depleted steranes originated from precursors that by ~36% relative to the reactant carbon. This carried a 3-hydroxyl group and unsatu- isotopic discrimination is in the range ration in the tetracyclic ring system, as observed for the difference in δ13C values of extant sterols do. Thus, there is no evidence coexisting carbonate minerals and organic for major changes in the known record of matter in some Archean deposits. This find- chemical fossils that could be attributed to ing emphasizes the importance of under- the inception, evolution, or alternative lipid standing the depositional context (e.g., biosynthetic pathways to the 24-alkylated sedimentary versus hydrothermal) of this steroids or hopanoids (Kopp et al. 2005). very ancient carbonaceous matter when Accordingly, if biomarkers that have been assessing its biogenicity. identified are confirmed to be indigenous We conclude that the origin of life predates to late Archean rocks, this will constitute the known record of preserved sedimentary robust evidence for the presence of algae rocks, but the nature of that life—and, in and bacteria early in Earth history. The particular, the nature of primary produc- fact that molecular oxygen is an absolute ers in the oceans—remains uncertain. All requirement for the biosynthesis of algal known geobiological records from Archean sterols also implies that oxygenic photosyn- rocks are consistent with an early evolution thesis must have been present at the time of cyanobacteria, but few if any require such (Summons et al. 2006). an interpretation (Knoll 2003a). Indeed, The carbon isotopic abundances of Early Kopp et al. (2005) have hypothesized that Archean carbonates and organic matter cyanobacteria originated only in association are comparable to those of younger rocks, with the initial accumulation of free oxygen indicating fractionation like that impart- in the atmosphere, 2320–2450 Ma (Holland ed by Rubisco-based autotrophy. Indeed, 2006). Careful geobiological analyses of C-isotopic signatures that are consistent with well-preserved Archean rocks remain a carbon fixation by Rubisco extend backward priority for continuing research.

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VI. CONCLUSIONS oceans. Prior to the proliferation of eukary- otic algae, cyanobacteria would, of course, In combination, paleontological and have had an open playing field, flourishing organic geochemical data suggest that the in oxygenated surface waters from coast- second half of Earth history can be divided line to mid-ocean gyres, although ceding into three major eras, with respect to marine deeper, at least intermittently euxinic parts photosynthesis. Limited data from Paleo- of the photic zone to green and purple pho- proterozoic and Mesoproterozoic rocks tosynthetic bacteria. Why, however, does suggest that cyanobacteria and other pho- it appear that cyanobacteria continued as tosynthetic bacteria dominated primary dominant features of the photosynthetic production at that time, with anoxygenic biota on continental shelves long after red photosynthetic bacteria playing an impor- and green algae entered the oceans? At least tant role at least locally in water masses in part, the answer may have to do with subtended by a euxinic oxygen-minimum the nutrient structure of oceans in which, zone. Indeed, available data suggest that beneath an oxygenated surface layer, the cyanobacteria continued as principal pho- oxygen minimum zone (Brocks et al. 2005), toautotrophs well into the Phanerozoic Eon if not the entire deep ocean (Canfield, and long after photosynthesis originated 1998), had a high propensity for developing

in eukaryotic cells. C29 sterane abundances euxinia. Under these conditions, one would indicate that green algae joined but did not expect little fixed N to resurface during entirely displace cyanobacteria as major upwelling (Anbar and Knoll 2002; Fennel et al. primary producers during the latest Prot- 2005), providing strong selective advantage erozoic and Cambrian; the second phase of for cyanobacteria able to fix N and scavenge primary production history thus initiated low concentrations of fixed N effectively persisted until the Mesozoic radiation of from . modern phytoplankton dominants. Later Increasing oxygenation of the oceans Triassic oceans may have been the first in during the Neoproterozoic Era (Canfield which cyanobacteria played a relatively et al. 2006; Fike et al. 2006) would have minor role in continental shelf production. begun to alleviate the N budget, as the mid- (Of course, they remain important today level waters that source upwelling would in the open gyre systems little recorded by have been increasingly likely to remain pre-Jurassic sedimentary rocks.) The degree oxic, limiting denitrification and anammox to which Chl a+c algae participated in Neo- reactions that strip fixed N from ascend- proterozoic and Paleozoic marine ecosys- ing anoxic water masses. More ammonium tems remains unresolved, but if present would have been returned to the surface, their role must be have much smaller than it and nitrate would have begun to accu- has been during the past 200 million years. mulate for the first time. In consequence, The observation that the oceans have eukaryotes would have spread more com- experienced two major shifts over the past pletely across benthic environments and billion years in the composition of primary into the phytoplankton, as recorded in the producers, and the corollary that at least geological record (Knoll et al. 2006). some clades emerged as ecologically domi- Dinoflagellates, diatoms, and coccolitho- nant primary producers long after their phorids exhibit many features that collectively evolutionary origin invites discussion of account for their ecological success in mod- possible drivers. The importance of cyano- ern oceans (Delwiche 2006; de Vargas et al. bacteria in Proterozoic primary production 2006; Kooistra et al. 2006). Why, then, do can be attributed to at least two circum- we not see evidence for similar success in stances, their early diversification and envi- Paleozoic seas? One possibility is that the ronmental circumstances in Proterozoic secondary endosymbioses that led to these

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group groups took place only at the begin- biota provide an important framework and ning of the Mesozoic Era or shortly earlier. stimulus for continuing paleobiological Such a scenario is consistent with clade- investigations of evolution. Latest specific molecular clocks for diatoms and Proterozoic and Cambrian phytoplankton coccolithophorids but is inconsistent with radiation may not simply be a response the hypothesis that secondary endosym- to animal evolution (e.g., Peterson and biosis involving red algal photosymbionts Butterfield 2005) but also a driver. Well- occurred only once, in the early history of documented (Bambach 1993) increases in the chromalveoates (Hackett et al. 2006). body size among Mesozoic (versus Paleo- Regardless of the timing of clade origina- zoic) marine invertebrates may reflect the tion, however, we need to consider environ- Mesozoic radiation of larger net plankton, mental factors, for the simple reason that while the so-called Mesozoic Marine Revo- it is hard to conceive of biological barriers lution among mostly Cretaceous and Ceno- would have prevented secondary endo- zoic marine animals may specifically reflect symbiosis long before the Mesozoic began. the rise to ecological prominence of diatoms Black shale distributions may provide (see Finkel 2006). Vermeij (1977) first docu- [AU4] perspective on this issue. Multiregional to mented the major evolutionary changes in globally widespread black shales are essen- skeletonized marine fauna during this inter- tially absent from Cenozoic successions, but val and ascribed it to a late Mesozoic radia- occur at about seven discrete stratigraphic tion of predators able to penetrate shells. horizons in the Mesozoic record (Jones and Bambach (1993), however, argued that the Jenkyns 2001). In contrast, there are at least required radiation of top predators could seven black shale horizons in the Devonian only occur as a consequence of increased record alone and many more in other parts primary production and, hence, increas- of the Paleozoic, especially the Cambrian ing nutrient status in the oceans. Bambach and Ordovician (Berry and Wilde 1978). (1993) suggested that evolving angiosperms Prior to the dawn of the Cambrian, most increased nutrient fluxes to the oceans, and shales were carbonaceous (e.g., Knoll and although this likely did occur (see Knoll Swett 1990; Abbott and Sweet 2000). If the 2003c), the evolution of a high-quality food redox structure of the oceans influenced the source and efficient nutrient transporter in selective environment of green versus Chl the form of diatoms likely played at least an a+c phytoplankton, then it may be that only equal role. in Mesozoic oceans did environmental con- ditions routinely favor the latter. As noted A. Directions for Continuing Research previously, fossils and biomarkers indicate that greens and cyanobacteria transiently Over the past decade, both paleontolo- reestablished themselves as principal pri- gists and organic geochemists have made mary producers during the Mesozoic OAEs; inroads into problems of photosynthetic his- green sulfur bacteria also proliferated dur- tory. Nonetheless, there continue to be more ing episodes of photic zone euxinia. Moreo- questions than answers. Future research ver, unlike chromalveolate photoautotrophs, will require more and independent studies both green algae and cyanobacteria show a of fossils and hydrocarbon distribution on pronounced preference for ammonium over Archean and Proterozoic rocks. However, it [AU3] nitrate in metabolism (Litchman 2006). Thus, will also require phylogenetic, biosynthetic, the long-term redox evolution of the oceans and functional studies of sterols and BHPs may govern the composition of marine (especially 2-Me-BHP) in living organisms primary producers through time. that will increase our ability to interpret Whatever their drivers, the two observed ancient records. In comparable fashion, con- transitions in the marine photosynthetic tinuing research on Proterozoic and Paleo-

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