Brian N. Popp

Compound-specific isotopic analyses: A novel tool for reconstruction of ancient biogeochemical processes

Patterns of isotopic fractionation in biogeochemical processes are reviewed and it is suggested that isotopic fractionations will be small when substrates are large. If so, isotopic compositions of biomarkers will reflect those of their biosynthetic precursors. This prediction is tested by consideration of results of analyses of geoporphyrins and geolipids from the Greenhorn Formation (Cretaceous, Western Interior Seaway of North America) and the Messel Shale (Eocene, lacustrine, southern Germany). It is shown (i) that isotopic compositions of porphyrins that are related to a common source, but which have been altered structurally, cluster tightly and (ii) that isotopic differences between geolipids and porphyrins related to a common source are equal to those observed in modern biosynthetic products. Both of these observations are consistent with preservation of biologically controlled isotopic compositions during diagenesis. Isotopic compositions of individual compounds can thus be interpreted in terms of biogeochemical processes in ancient depositional environments. In the Cretaceous samples, isotopic compositions of n-alkanes are covariant with those of total organic carbon, while delta values for pristane and phytane are covariant with those of porphyrins. In this unit representing an open marine environment, the preserved acyclic polyisoprenoids apparently derive mainly from primary material, while the extractable, n-alkanes derive mainly from lower levels of the food chain. In the Messel Shale, isotopic compositions of individual biomarkers range from -20.9 to -73.4% vs PDB. Isotopic compositions of specific compounds can be interpreted in terms of origin from methylotrophic, chemautotrophic, and chemolithotrophic microorganisms as well as from primary producers that lived in the water column and sediments of this ancient lake.

Dependence of phytoplankton carbon isotopic composition on growth rate and [CO2)aq: Theoretical considerations and experimental results

The carbon isotopic composition of the marine diatom Phaeodactylum tricornutum (δ13Cp) was measured over a series of growth rates (μ) in a continuous culture system in which both δ133CCO2 and [CO2]aq were determined. In accord with theory, a linear relationship was found to exist between μ/ [CO2]aq and ɛp (≡1000(δ13CCO2 − δ13Cp)/1000 + d δ13Cp), the biological fractionation associated with carbon fixation. The range of [CO2]aq in the continuous culture system was 13–31 μmol kg−1. Measurements of δ13CCO2 and [CO2]aq in the mixed layer of the equatorial Pacific and estimates of δ13Cp obtained from the δ13C of chlorophyll a combined with the regression line fit to the P. tricornutum data give phytoplankton growth rates that are in excellent agreement with those estimated via other techniques. Measurement of ɛp and [CO2]aq in the field can provide an estimate of in situ phytoplankton growth rates without the potential artifacts associated with incubation methodologies. These findings also suggest that accurate estimations of ancient CO2(aq) concentrations will require knowledge of both ɛp and phytoplankton growth rate.

Effect of Phytoplankton Cell Geometry on Carbon Isotopic Fractionation

The carbon isotopic compositions of the marine diatom Porosira glacialis and the marine cyanobacterium Synechococcus sp. were measured over a series of growth rates (μ) in a continuous culture system in which the concentration and carbon isotopic composition of CO2(aq) were determined. These data were compared with previously published isotopic results of growth rate experiments using the marine diatom Phaeodactylum tricornutum and the marine haptophyte Emiliania huxleyi. Systematic relationships were found to exist between μ/[CO2(aq)] and carbon isotopic fractionation (ϵP) for each species. Maximum isotopic fractionation (ϵf) for P. glacialis, E. huxleyi, and P. tricornutum was ∼25‰, suggesting that this value may be typical for maximum fractionation associated with Rubisco and β-carboxylases for marine eukaryotic algae. By contrast, ϵf determined for Synechococcus clone CCMP838 was ∼7‰ lower. The slopes of the lines describing the relationship between ϵP and μ/[CO2(aq)] for eukaryotic algal species were different by a factor of more than 20. This result can be accounted for by differences in the surface area and cellular carbon content of the cells. Comparison of chemostat experimental results with calculated results using a diffusion based model imply that the algae in the experiments were actively transporting inorganic carbon across the cell membrane. Our results suggest that accurate estimates of paleo-[CO2(aq)] from ϵP measured in sediments will require knowledge of growth rate as well as cell surface area and either cell carbon quota or cell volume. Given growth rate estimates, our empirical relationship permits reliable calculations of paleo-[CO2(aq)] using compound-specific isotopic analyses of C37 alkadienones (select haptophytes) or fossilized frustules (diatoms).

Brachiopods as indicators of original isotopic compositions in some Paleozoic limestones

The original stable isotopic composition of Paleozoic marine carbonate rocks is important to establish a baseline for evaluating diagenetic alteration and providing a reliable data-base for modeling exogenic geochemical cycles of the elements. We have compared the δ 18 O and δ 13 C values in the nonluminescent portions of brachiopods with similar published data of whole brachiopods, other whole fossils, and estimates of original isotopic composition of marine cements. The oxygen and carbon isotopic records for each of these Paleozoic components show generally good internal consistency. Significant discrepancies, however, were noted between results on the different components. Isotopic and trace-element data presented in this study suggest that Permo-Carboniferous whole brachiopods are little altered chemically. Nonetheless, a more reliable (but not fool-proof) approach for obtaining pristine isotopic values is microsampling of “least-altered” regions based on cathodoluminescence in conjunction with staining techniques and elemental analyses. The carbon and oxygen isotopic compositions of all components decrease in δ 18 O and δ 13 C in geologically older material. Neither temporal trend is monotonic, however. Oxygen isotopic results suggest an important positive shift in δ 18 O of about 2‰ during the early Carboniferous, whereas the carbon isotope trend shows a major positive shift (≈2%–3‰) during the mid-Carboniferous.

Consistent fractionation of 13C in nature and in the laboratory: Growth‐rate effects in some haptophyte algae

The carbon isotopic fractionation accompanying formation of biomass by alkenone-producing algae in natural marine environments varies systematically with the concentration of dissolved phosphate. Specifically, if the fractionation is expressed by epsilon p approximately delta e - delta p, where delta e and delta p are the delta 13C values for dissolved CO2 and for algal biomass (determined by isotopic analysis of C37 alkadienones), respectively, and if Ce is the concentration of dissolved CO2, micromole kg-1, then b = 38 + 160*[PO4], where [PO4] is the concentration of dissolved phosphate, microM, and b = (25 - epsilon p)Ce. The correlation found between b and [PO4] is due to effects linking nutrient levels to growth rates and cellular carbon budgets for alkenone-containing algae, most likely by trace-metal limitations on algal growth. The relationship reported here is characteristic of 39 samples (r2 = 0.95) from the Santa Monica Basin (six different times during the annual cycle), the equatorial Pacific (boreal spring and fall cruises as well as during an iron-enrichment experiment), and the Peru upwelling zone. Points representative of samples from the Sargasso Sea ([PO4] < or = 0.1 microM) fall above the b = f[PO4] line. Analysis of correlations expected between mu (growth rate), epsilon p, and Ce shows that, for our entire data set, most variations in epsilon p result from variations in mu rather than Ce. Accordingly, before concentrations of dissolved CO2 can be estimated from isotopic fractionations, some means of accounting for variations in growth rate must be found, perhaps by drawing on relationships between [PO4] and Cd/Ca ratios in shells of planktonic foraminifera.

Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California

Nitrification plays an important role in marine biogeochemistry, yet efforts to link this process to the microorganisms that mediate it are surprisingly limited. In particular, ammonia oxidation is the first and rate-limiting step of nitrification, yet ammonia oxidation rates and the abundance of ammonia-oxidizing bacteria (AOB) have rarely been measured in tandem. Ammonia oxidation rates have not been directly quantified in conjunction with ammonia-oxidizing archaea (AOA), although mounting evidence indicates that marine Crenarchaeota are capable of ammonia oxidation, and they are among the most abundant microbial groups in the ocean. Here, we have directly quantified ammonia oxidation rates by 15N labeling, and AOA and AOB abundances by quantitative PCR analysis of ammonia monooxygenase subunit A (amoA) genes, in the Gulf of California. Based on markedly different archaeal amoA sequence types in the upper water column (60 m) and oxygen minimum zone (OMZ; 450 m), novel amoA PCR primers were designed to specifically target and quantify ‘shallow’ (group A) and ‘deep’ (group B) clades. These primers recovered extensive variability with depth. Within the OMZ, AOA were most abundant where nitrification may be coupled to denitrification. In the upper water column, group A tracked variations in nitrogen biogeochemistry with depth and between basins, whereas AOB were present in relatively low numbers or undetectable. Overall, 15NH4+ oxidation rates were remarkably well correlated with AOA group A amoA gene copies (r2=0.90, P<0.001), and with 16S rRNA gene copies from marine Crenarchaeota (r2=0.85, P<0.005). These findings represent compelling evidence for an archaeal role in oceanic nitrification.

An isotopic study of biogeochemical relationships between carbonates and organic carbon in the Greenhorn Formation

Carbon-isotopic compositions of total carbonate, inoceramid carbonate, micritic carbonate, secondary cements, total organic carbon, and geoporphyrins have been measured in 76 different beds within a 17-m interval of a core through the Greenhorn Formation, an interbedded limestone and calcareous shale unit of Cretaceous age (Cenomanian-Turonian) from the Western Interior Seaway of North America. Results are considered in terms of variations in the processes of primary production (which led to the biosynthesis of the molecular precursors of the geoporphyrins) and in secondary processes (those mediating the transformation of primary organic material into sedimentary total organic carbon). It is shown that the porphyrin isotopic record reflects primary isotopic variations more closely than the TOC isotopic record, and that, in these sediments, TOC is enriched in 13C relative to its primary precursor by 0.6 to 2.8%. This enrichment is attributed to isotope effects within the consumer foodweb and is associated with respiratory heterotrophy. Variations in this secondary enrichment are correlated with variations in the isotopic composition of marine carbonate. This correlation is attributed to effects of environmental changes on the marine foodweb. These may have included increased atmospheric oxygen associated with the Cenomanian-Turonian oceanic anoxic event. The isotopic fractionation associated with fixation of carbon by primary producers is observed to have varied by 1.5% during the interval of deposition. It is suggested that this change is due to a variation in the makeup of the community of primary producers and/or to a decrease in the atmospheric abundance of CO2 during the oceanic anoxic event.

Global declines in oceanic nitrification rates as a consequence of ocean acidification

Ocean acidification produced by dissolution of anthropogenic carbon dioxide (CO2) emissions in seawater has profound consequences for marine ecology and biogeochemistry. The oceans have absorbed one-third of CO2 emissions over the past two centuries, altering ocean chemistry, reducing seawater pH, and affecting marine animals and phytoplankton in multiple ways. Microbially mediated ocean biogeochemical processes will be pivotal in determining how the earth system responds to global environmental change; however, how they may be altered by ocean acidification is largely unknown. We show here that microbial nitrification rates decreased in every instance when pH was experimentally reduced (by 0.05–0.14) at multiple locations in the Atlantic and Pacific Oceans. Nitrification is a central process in the nitrogen cycle that produces both the greenhouse gas nitrous oxide and oxidized forms of nitrogen used by phytoplankton and other microorganisms in the sea; at the Bermuda Atlantic Time Series and Hawaii Ocean Time-series sites, experimental acidification decreased ammonia oxidation rates by 38% and 36%. Ammonia oxidation rates were also strongly and inversely correlated with pH along a gradient produced in the oligotrophic Sargasso Sea (r2 = 0.87, P < 0.05). Across all experiments, rates declined by 8–38% in low pH treatments, and the greatest absolute decrease occurred where rates were highest off the California coast. Collectively our results suggest that ocean acidification could reduce nitrification rates by 3–44% within the next few decades, affecting oceanic nitrous oxide production, reducing supplies of oxidized nitrogen in the upper layers of the ocean, and fundamentally altering nitrogen cycling in the sea.

A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters

Nitrous oxide (N2O), a trace gas whose concentration is increasing in the atmosphere, plays an important role in both radiative forcing and stratospheric ozone depletion,. Its biogeochemical cycle has thus come under intense scrutiny in recent years. Despite these efforts, the global budget of N2O remains unresolved, and the nature and magnitude of the sources and sinks continue to be debated despite the constraints that can be provided by characterizations of the gas,. We report here the results of dual-isotope measurements of N2O from the water column of the subtropical North Pacific Ocean. Nitrous oxide within the lower-euphotic and upper-aphotic zones is depleted in both 15N and 18O relative to its tropospheric and deep-ocean composition. These findings are consistent with a prediction, based on global mass-balance considerations, of a near-surface isotopically depleted oceanic N2O source. Our results indicate that this source, probably produced by bacterial nitrification, contributes significantly to the ocean–atmosphere flux of N2O in the oligotrophic subtropical North Pacific Ocean. This source may act to buffer the isotopic composition of tropospheric N2O, and is quantitatively significant in the global tropospheric N2O budget. Because dissolved gases in near-surface waters are more readily exchanged with the atmospheric reservoir than those in deep waters, the existence of a quantitatively significant N2O source at a relatively shallow depth has potentially important implications for the susceptibility of the source, and the ocean–atmosphere flux, to climatic influences.

87Sr/86Sr ratios in Permo-Carboniferous sea water from the analyses of well-preserved brachiopod shells

Abstract Sr isotopic analyses of well-preserved portions of Permo-Carboniferous brachiopods distributed globally confirm the general shape of the Sr isotope age curve established by previous workers for this time interval. There is little variation between the Sr isotopic composition of unaltered portions of brachiopods and that of portions of the same shell interpreted to be diagenetically altered (based on cathodoluminescence, elemental, and stable isotopic data). However, the Sr isotopic composition in diagenetically altered micritic matrix adjacent to the shell is more radiogenic. The Sr isotopic composition in the unaltered portions of calcitic megafossils has potential as a stratigraphie tool.