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The Geological Succession of Primary Producers in the Oceans

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The Geological Succession of Primary Producers in the Oceans 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. Microfossils B. Molecular Biomarkers II. The Rise of Modern Phytoplankton A. Fossils and Phylogeny B. Biomarkers and the Rise of Modern Phytoplankton C. Summary of the Rise of Modern Phytoplankton III. Paleozoic Primary Production A. Microfossils B. Paleozoic Molecular Biomarkers C. Paleozoic Summary IV. Proterozoic Primary Production A. Prokaryotic Fossils B. Eukaryotic Fossils C. Proterozoic Molecular Biomarkers D. Summary of the Proterozoic Record V. Archean Oceans VI. Conclusions A. Directions for Continuing Research References In the modern oceans, diatoms, dinoflagel- geobiological prominence only in the Mesozoic 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 photosynthesis 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 CCh08-P370518.inddh08-P370518.indd 113333 55/2/2007/2/2007 11:16:46:16:46 PPMM 134 8. THE GEOLOGICAL SUCCESSION OF PRIMARY PRODUCERS IN THE OCEANS fossils and molecular biomarkers. Because without well developed frustules might these two windows on ancient biology 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 bacteria have a relatively high probability reflects evolutionary history. of entering the fossil 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 picoplankton such as Prochlorococcus are unlikely to leave recognizable body (or, as A. Microfossils it turns out, molecular) fossils. A number of algal clades include good candidates for fos- Microfossils, preserved as organic cell silization, especially groups with distinctive walls or mineralized tests and scales, record resting stages (phycomate prasinophytes, the morphologies and (viewed via transmis- dinoflagellates) or mineralized skeletons sion electron microscopy) ultrastructures of (diatoms, coccolithophorids, coralline reds, ancient microorganisms. Such fossils can caulerpalean and dasyclad greens). Other provide unambiguous records of phyto- primary producers fossilize occasionally, but plankton in past oceans—diatom 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 dinocysts, 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 dinoflagellate 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 Jurassic 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 organisms can be incorporated CCh08-P370518.inddh08-P370518.indd 113434 55/2/2007/2/2007 11:16:46:16:46 PPMM I. RECORDS OF PRIMARY PRODUCERS IN ANCIENT OCEANS 135 into sediments and ultimately into sedimen- can remain recognizable as the products of tary rocks that can survive for billions of years. 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-year time scales under ideal conditions kers ranges from species to domain 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 chlorophyll 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
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