The origin of carbon isotope vital effects in coccolith calcite.

Calcite microfossils are widely used to study climate and oceanography in Earth's geological past. Coccoliths, readily preserved calcite plates produced by a group of single-celled surface-ocean dwelling algae called coccolithophores, have formed a significant fraction of marine sediments since the Late Triassic. However, unlike the shells of foraminifera, their zooplankton counterparts, coccoliths remain underused in palaeo-reconstructions. Precipitated in an intracellular chemical and isotopic microenvironment, coccolith calcite exhibits large and enigmatic departures from the isotopic composition of abiogenic calcite, known as vital effects. Here we show that the calcification to carbon fixation ratio determines whether coccolith calcite is isotopically heavier or lighter than abiogenic calcite, and that the size of the deviation is determined by the degree of carbon utilization. We discuss the theoretical potential for, and current limitations of, coccolith-based CO2 paleobarometry, that may eventually facilitate use of the ubiquitous and geologically extensive sedimentary archive.

Calcification response of a key phytoplankton family to millennial-scale environmental change.

Coccolithophores are single-celled photosynthesizing marine algae, responsible for half of the calcification in the surface ocean, and exert a strong influence on the distribution of carbon among global reservoirs, and thus Earth's climate. Calcification in the surface ocean decreases the buffering capacity of seawater for CO2, whilst photosynthetic carbon fixation has the opposite effect. Experiments in culture have suggested that coccolithophore calcification decreases under high CO2 concentrations ([CO2(aq)]) constituting a negative feedback. However, the extent to which these results are representative of natural populations, and of the response over more than a few hundred generations is unclear. Here we describe and apply a novel rationale for size-normalizing the mass of the calcite plates produced by the most abundant family of coccolithophores, the Noëlaerhabdaceae. On average, ancient populations subjected to coupled gradual increases in [CO2(aq)] and temperature over a few million generations in a natural environment become relatively more highly calcified, implying a positive climatic feedback. We hypothesize that this is the result of selection manifest in natural populations over millennial timescales, so has necessarily eluded laboratory experiments.

Goldilocks and the three inorganic equilibria: how Earth's chemistry and life coevolve to be nearly in tune.

Life and the chemical environment are united in an inescapable feedback cycle. The periodic table of the elements essential for life has transformed over Earth's history, but, as today, evolved in tune with the elements available in abundance in the environment. The most revolutionary time in life's history was the advent and proliferation of oxygenic photosynthesis which forced the environment towards a greater degree of oxidation. Consideration of three inorganic chemical equilibria throughout this gradual oxygenation prescribes a phased release of trace metals to the environment, which appear to have coevolved with employment of these new chemicals by life. Evolution towards complexity was chemically constrained, and changes in availability of notably Fe, Zn and Cu paced the systematic development of complex organisms. Evolving life repeatedly catalysed its own chemical challenges via the unwitting release of new and initially toxic chemicals. Ultimately, the harnessing of these allowed life to advance to greater complexity, though the mechanism responsible for translating novel chemistry to heritable use remains elusive. Whether a chemical acts as a poison or a nutrient lies both in the dose and in its environmental history.

Thermal, trophic and metabolic life histories of inaccessible fishes revealed from stable-isotope analyses: a case study using orange roughy Hoplostethus atlanticus.

A time-resolved record of inhabited water depth, metabolic rate and trophic behaviour of the orange roughy Hoplostethus atlanticus was recovered from combined stable-isotope analyses of otolith and muscle tissue. The results demonstrate that H. atlanticus from the north-east Atlantic Ocean have a complex life history with three distinct depth-stratified life stages. Early juvenile H. atlanticus occupy relatively shallow habitats, juvenile H. atlanticus show a deep-demersal phase, rising at sexual maturity, and adult H. atlanticus exploit increasingly deep habitats with increasing age. At all sampled sizes, H. atlanticus muscle tissues have an isotopic composition suggesting a benthic rather than benthopelagic or pelagic diet. Isotopic measures of relative metabolic rate provide an insight into energy partitioning throughout ontogeny. Hoplostethus atlanticus have relatively low metabolic rates compared to coexisting deep-water benthic fishes, consistent with their unusually high longevity. Surprisingly, lifetime fastest growth rates are achieved during juvenile stages when otolith isotopes imply deep-water residency and relatively low metabolic rates. Fast growth may be sustained during a period of high efficiency associated with reduced metabolic costs of prey capture or predator evasion. The stable-isotope approach can be applied to any teleost and provides a rapid, cost-effective technique for studying deep-water fish communities.

Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide.

Rubisco, the most abundant enzyme on the Earth and responsible for all photosynthetic carbon fixation, is often thought of as a highly conserved and sluggish enzyme. Yet, different algal Rubiscos demonstrate a range of kinetic properties hinting at a history of evolution and adaptation. Here, we show that algal Rubisco has indeed evolved adaptively during ancient and distinct geological periods. Using DNA sequences of extant marine algae of the red and Chromista lineage, we define positive selection within the large subunit of Rubisco, encoded by rbcL, to occur basal to the radiation of modern marine groups. This signal of positive selection appears to be responding to changing intracellular concentrations of carbon dioxide (CO(2)) triggered by physiological adaptations to declining atmospheric CO(2). Within the ecologically important Haptophyta (including coccolithophores) and Bacillariophyta (diatoms), positive selection occurred consistently during periods of falling Phanerozoic CO(2) and suggests emergence of carbon-concentrating mechanisms. During the Proterozoic, a strong signal of positive selection after secondary endosymbiosis occurs at the origin of the Chromista lineage (approx. 1.1 Ga), with further positive selection events until 0.41 Ga, implying a significant and continuous decrease in atmospheric CO(2) encompassing the Cryogenian Snowball Earth events. We surmise that positive selection in Rubisco has been caused by declines in atmospheric CO(2) and hence acts as a proxy for ancient atmospheric CO(2).

Interaction of the coccolithophore Gephyrocapsa oceanica with its carbon environment: response to a recreated high-CO2 geological past.

Coccolithophores have played a key role in the carbon cycle since becoming dominant in the Cretaceous ocean, and their influence depends fundamentally on how they interact with their external carbon environment. Because the photosynthetic carbon-fixing enzyme Rubisco requires high levels of CO(2) for effective catalysis, coccolithophores are known to induce carbon concentrating mechanisms (CCMs) to raise the level of dissolved inorganic carbon (DIC) in an 'internal pool'. The ocean carbon system has varied greatly over the geological past, suggesting that coccolithophore interactions with that external carbon environment will have changed in parallel. The widespread present-day coccolithophore Gephyrocapsa oceanica was acclimated here to a geological scale change in the seawater carbon system (five times higher DIC and alkalinity). Significant acclimation in response to the external carbon environment was demonstrated by a fourfold increase in the K(m) substrate concentration requirement for half-maximum photosynthetic carbon fixation rates (suggesting that CCMs were down-regulated when ambient carbon was more available). There was, however, no difference in growth rate, morphology or calcification, suggesting that calcification is not coupled to photosynthesis as one of the CCMs induced here and that productivity (growth rate and calcification) is not carbon-limited under representative present-day conditions. Beyond the kinetic parameters of photosynthesis, the only other indication of changed cell physiology seen was the increased fractionation of carbon isotopes into organic matter. These findings demonstrate that G. oceanica changes its carbon-use physiology to maintain consistent photosynthetic carbon fixation in concert with different levels of ambient DIC without changing its morphology or calcification.

Sensitivity of coccolithophores to carbonate chemistry and ocean acidification.

About one-third of the carbon dioxide (CO(2)) released into the atmosphere as a result of human activity has been absorbed by the oceans, where it partitions into the constituent ions of carbonic acid. This leads to ocean acidification, one of the major threats to marine ecosystems and particularly to calcifying organisms such as corals, foraminifera and coccolithophores. Coccolithophores are abundant phytoplankton that are responsible for a large part of modern oceanic carbonate production. Culture experiments investigating the physiological response of coccolithophore calcification to increased CO(2) have yielded contradictory results between and even within species. Here we quantified the calcite mass of dominant coccolithophores in the present ocean and over the past forty thousand years, and found a marked pattern of decreasing calcification with increasing partial pressure of CO(2) and concomitant decreasing concentrations of CO(3)(2-). Our analyses revealed that differentially calcified species and morphotypes are distributed in the ocean according to carbonate chemistry. A substantial impact on the marine carbon cycle might be expected upon extrapolation of this correlation to predicted ocean acidification in the future. However, our discovery of a heavily calcified Emiliania huxleyi morphotype in modern waters with low pH highlights the complexity of assemblage-level responses to environmental forcing factors.

Cool La Niña during the warmth of the Pliocene?

The role of El Niño-Southern Oscillation (ENSO) in greenhouse warming and climate change remains controversial. During the warmth of the early-mid Pliocene, we find evidence for enhanced thermocline tilt and cold upwelling in the equatorial Pacific, consistent with the prevalence of a La Niña-like state, rather than the proposed persistent warm El Niño-like conditions. Our Pliocene paleothermometer supports the idea of a dynamic "ocean thermostat" in which heating of the tropical Pacific leads to a cooling of the east equatorial Pacific and a La Niña-like state, analogous to observations of a transient increasing east-west sea surface temperature gradient in the 20th-century tropical Pacific.