A general model for carbon isotopes in red-lineage phytoplankton: Interplay between unidirectional processes and fractionation by RubisCO

Wilkes, Elise B.; Pearson, Ann

doi:10.1016/j.gca.2019.08.043

Cited by 51 publications

(86 citation statements)

References 130 publications

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“…Yet, there is a large difference between in vitro ε RuBisCO of Emiliania huxleyi and the maximum in vivo whole cell biomass carbon isotopic fractionation of 24‰ observed under high CO 2 conditions, nitrate‐limited growth experiments (Bidigare et al , ) or 21.5‰ in E. huxleyi grown in chemostats (Wilkes et al , ), as well as estimates of fractionation from coccolithophores of up to 24‰ from biomarkers isolated from middle‐to‐late Eocene sediments, a time of presumed high pCO 2 (Pagani et al , ). The difference in in vivo and in vitro fractionation may alternatively result from novel comparable magnitude additional fractionation effects either upstream or downstream of the RuBisCO enzyme in the inorganic carbon utilization mechanisms used by this organism (Tsuji et al , ; Wilkes and Pearson, ).…”

Section: Stable Isotopic Fractionation As a Tracer Of Rubisco Evolutimentioning

confidence: 99%

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

et al. 2020

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Summary RuBisCO‐catalyzed CO2 fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500 Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5‐bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen‐rich atmosphere promoted the appearance of CO2 concentrating mechanisms (CCMs) and/or the evolution of a more CO2‐specific RuBisCO enzyme. The wide variability in RuBisCO kinetic traits of extant organisms reveals a history of adaptation to the prevailing CO2/O2 concentrations and the thermal environment throughout evolution. Notable differences in the kinetic parameters are found among the different forms of RuBisCO, but the differences are also associated with the presence and type of CCMs within each form, indicative of co‐evolution of RuBisCO and CCMs. Trade‐offs between RuBisCO kinetic traits vary among the RuBisCO forms and also among phylogenetic groups within the same form. These results suggest that different biochemical and structural constraints have operated on each type of RuBisCO during evolution, probably reflecting different environmental selective pressures. In a similar way, variations in carbon isotopic fractionation of the enzyme point to significant differences in its relationship to the CO2 specificity among different RuBisCO forms. A deeper knowledge of the natural variability of RuBisCO catalytic traits and the chemical mechanism of RuBisCO carboxylation and oxygenation reactions raises the possibility of finding unrevealed landscapes in RuBisCO evolution.

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Section: Stable Isotopic Fractionation As a Tracer Of Rubisco Evolutimentioning

confidence: 99%

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

et al. 2020

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“…Conversely, targeted studies of individual photosynthetic taxa or biomarkers have sometimes suggested a pattern of increasing or unchanging δ 13 C values over increasing depth in the euphotic zone (Prahl et al, 2005;Popp et al, 2006;Tolosa et al, 2008;Radabaugh et al, 2014). The recent model of Wilkes and Pearson (2019) suggests that increasing δ 13 C values over depth could be a phenomenon specific to eukaryotic phytoplankton with intracellular CO 2 partitioning or carbon concentrating strategies, with carbon isotopic fractionation varying according to whether growth is limited by low nutrient concentrations (upper euphotic zone/mixed layer) or other factors such as light [lower euphotic zone/upper pycnocline; also explored by Laws et al (2002) and Cassar et al (2006)]. Some phytoplankton also employ active uptake and/or fixation of bicarbonate (HCO 3 − ), thereby also complicating relationships between cell size, CO 2 concentrations, and δ 13 C P (e.g., Bentaleb et al, 1998;Cassar et al, 2004).…”

Section: Photosynthetic Hypotheses For Origins Of Low δ 13 C Poc Valumentioning

confidence: 99%

“…To explain the δ 13 C POC variations, the expressed isotopic fractionation (ε P ) between CO 2 (δ 13 C CO2 ) and photosynthetic biomass (δ 13 C P ) (Hayes, 1993(Hayes, , 2001) was found to correlate to some degree with CO 2 concentration, but also with phytoplankton growth rates and cell geometry (Laws et al, 1995;Popp et al, 1998, and others). Additional influence on ε P can arise from the use of carbon concentrating mechanisms and the active uptake and/or fixation of bicarbonate (see Wilkes and Pearson, 2019).…”

Section: Introductionmentioning

confidence: 99%

Open-Ocean Minima in δ13C Values of Particulate Organic Carbon in the Lower Euphotic Zone

Henderson

2020

Front. Mar. Sci.

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Extensive studies in the 1980s-1990s led to the characterization of latitudinal variations in sea surface δ 13 C values of particulate organic carbon (δ 13 C POC), and relationships were found with CO 2 concentrations, temperature, growth rates, and cell geometries. Surprisingly, no large-scale efforts have been made to describe variations in δ 13 C POC values over depth in the water column. Here we compile published examples demonstrating a widespread isotopic pattern in particulate organic carbon (POC) of the upper water column. In 51 vertical profiles, δ 13 C POC values in the lower euphotic zone on average are 1.4 lower than δ 13 C POC values in the upper euphotic zone of open ocean settings. In a majority of locations this vertical decrease in δ 13 C POC values is >2 and up to 5 , larger than the commonly recognized vertical δ 13 C variation in dissolved inorganic carbon over the same depths. We briefly review hypotheses and supporting evidence offered by previous studies of individual water columns: The observed patterns could result from vertical differences in photosynthetic growth rates or community composition, biochemical composition of organic matter due to degradation, isotopic disequilibrium within the dissolved inorganic carbon pool, particle dynamics, or seasonal vertical mixing. Coordinated isotopic, biological, and seawater chemistry data are sparse, and consistent drivers of this widespread isotopic pattern are currently elusive. Further work is needed to adequately characterize the environmental conditions coinciding with this pattern, to test its origins, and to determine if the magnitude of upper water column δ 13 C POC variations could be a useful marker of upper ocean carbon cycle dynamics.

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“…where Ɛ f is the maximum isotopic fractionation due to CO 2 -fixation via the enzyme Rubisco, which has shown a sum range from 25 to 28‰ [17][18][19] . It should be noted that the very few in vivo Rubisco fractionation studies have much lower values 20,21 , which Wilkes and Pearson 22 suggest there may be due to multiple stages of fractionation instead of the singular Rubisco fractionation step. Several other studies have expanded on Eq.…”

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confidence: 99%

Testing algal-based pCO2 proxies at a modern CO2 seep (Vulcano, Italy)

Witkowski

Meer

Smit

et al. 2020

Sci Rep

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Understanding long-term trends in atmospheric concentrations of carbon dioxide (pco 2) has become increasingly relevant as modern concentrations surpass recent historic trends. one method for estimating past pco 2 , the stable carbon isotopic fractionation associated with photosynthesis (Ɛ p) has shown promise over the past several decades, in particular using species-specific biomarker lipids such as alkenones. Recently, the Ɛ p of more general biomarker lipids, organic compounds derived from a multitude of species, have been applied to generate longer-spanning, more ubiquitous records than those of alkenones but the sensitivity of this proxy to changes in pco 2 has not been constrained in modern settings. Here, we test Ɛ p using a variety of general biomarkers along a transect taken from a naturally occurring marine co 2 seep in Levante Bay of the Aeolian island of Vulcano in italy. the studied general biomarkers, loliolide, cholesterol, and phytol, all show increasing depletion in 13 c over the transect from the control site towards the seep, suggesting that co 2 exerts a strong control on isotopic fractionation in natural phytoplankton communities. the strongest shift in fractionation was seen in phytol, and pco 2 estimates derived from phytol confirm the utility of this biomarker as a proxy for pco 2 reconstruction. The concentration of atmospheric carbon dioxide (pCO 2 , expressed in partial pressure µatm), as directly measured from air trapped in ice cores, has had a major influence on climate over the past 800 thousand years (ka) 1. During this period, pCO 2 and temperature oscillated together between stable bounds every 100 ka 2. In the past two centuries, the rise of pCO 2 has broken those bounds from the pre-industrial values, previously only ranging between ca. 180 to 280 µatm, to the 410 µatm of today 3. This rapid rise in pCO 2 causes concern that climate, particularly temperature, will accordingly change. In order to better understand how changes may occur, reconstructing longer trends in pCO 2 over the geologic record could offer context for evaluating the direction and magnitude of climate change. Many proxies have been developed for reconstructing past pCO 2 and applied with mixed success over the past several decades 4. One method for studying past pCO 2 makes use of the stable carbon isotopic fractionation due to CO 2-fixation (Ɛ p), where biomass of photoautotrophs becomes increasingly depleted in 13 C as pCO 2 increases due to kinetic discrimination by the CO 2-fixing enzyme Rubisco 5-7. Ɛ p can be derived from the δ 13 C of photoautotrophic biomass, recorded in sedimentary organic matter, and the δ 13 C of inorganic CO 2 derived from the carbonate in the shells of planktonic foraminifera 8. Although pCO 2 has been shown to be one of the dominant physiological control on the δ 13 C of photoautotrophic biomass 9 , studies on Ɛ p in algae have shown that other factors may influence this value, primarily growth rate 10 and cell size and shape 11 , as well as minor influences such as light, and ...

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A general model for carbon isotopes in red-lineage phytoplankton: Interplay between unidirectional processes and fractionation by RubisCO

Cited by 51 publications

References 130 publications

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Open-Ocean Minima in δ13C Values of Particulate Organic Carbon in the Lower Euphotic Zone

Testing algal-based pCO2 proxies at a modern CO2 seep (Vulcano, Italy)

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A general model for carbon isotopes in red-lineage phytoplankton: Interplay between unidirectional processes and fractionation by RubisCO

Cited by 51 publications

References 130 publications

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO2 concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO2 concentrating mechanisms

Open-Ocean Minima in δ13C Values of Particulate Organic Carbon in the Lower Euphotic Zone

Testing algal-based pCO2 proxies at a modern CO2 seep (Vulcano, Italy)

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Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms