Sustained net CO2 evolution during photosynthesis by marine microorganism (original) (raw)

Massive light-dependent cycling of inorganic carbon between oxygenic photosynthetic microorganisms and their surroundings

2003

Membrane inlet mass spectrometry indicated massive light-dependent cycling of inorganic carbon between the medium and the cells of various phytoplankton species representing the main groups of aquatic primary producers. These included diatoms, symbiotic and free living dinoflagellates, a coccolithophorid, a green alga and filamentous and single cell cyanobacteria. These organisms could maintain an ambient CO 2 concentration substantially above or below that expected at chemical equilibrium with HCO 3 −. The coccolithophorid Emiliania huxleyi shifted from net CO 2 uptake to net CO 2 efflux with rising light intensity. Differing responses of CO 2 uptake and CO 2 fixation to changing light intensity supported the notion that these two processes are not compulsorily linked. Simultaneous measurements of CO 2 and O 2 exchange and of the fluorescence parameters in Synechococcus sp. strain PCC 7942, showed that CO 2 uptake can serve as a sensitive probe of the energy status of the photosynthetic reaction centers. However, during transitions in light intensity, changes in CO 2 uptake did not accord with those expected from fluorescence change. Quantification of the net fluxes of CO 2 , HCO 3 − and of photosynthesis at steady-state revealed that substantial HCO 3 − efflux accompanied CO 2 uptake and fixation in the case of 'CO 2 users'. On the other hand, 'HCO 3 − users' were characterized by a rate of net CO 2 uptake below that of CO 2 fixation. The results support the notion that entities associated with the CCM function not only in raising the CO 2 concentration at the site of Rubisco; they may also serve as a means of diminishing photodynamic damage by dissipating excess light energy. Abbreviations: CA-carbonic anhydrase; Ci-inorganic carbon; [CO 2(dis) ]-dissolved CO 2 concentration; MICC-massive inorganic carbon cycling

Evolving paradigms in biological carbon cycling in the ocean

National Science Review, 2018

Carbon is a keystone element in global biogeochemical cycles. It plays a fundamental role in biotic and abiotic processes in the ocean, which intertwine to mediate the chemistry and redox status of carbon in the ocean and the atmosphere. The interactions between abiotic and biogenic carbon (e.g. CO2, CaCO3, organic matter) in the ocean are complex, and there is a half-century-old enigma about the existence of a huge reservoir of recalcitrant dissolved organic carbon (RDOC) that equates to the magnitude of the pool of atmospheric CO2. The concepts of the biological carbon pump (BCP) and the microbial loop (ML) shaped our understanding of the marine carbon cycle. The more recent concept of the microbial carbon pump (MCP), which is closely connected to those of the BCP and the ML, explicitly considers the significance of the ocean's RDOC reservoir and provides a mechanistic framework for the exploration of its formation and persistence. Understanding of the MCP has benefited from a...

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

Oxygenic photosynthesis evolved at least 2.4 Ga; all oxygenic organisms use the ribulose bisphosphate carboxylase-oxygenase (Rubisco) -photosynthetic carbon reduction cycle (PCRC) rather than one of the five other known pathways of autotrophic CO 2 assimilation. The high CO 2 and (initially) O 2 -free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO 2 decreased and O 2 increased, Rubisco oxygenase activity increased and 2-phosphoglycolate was produced, with the evolution of pathways recycling this inhibitory product to sugar phosphates. Changed atmospheric composition also selected for Rubiscos with higher CO 2 affinity and CO 2 /O 2 selectivity correlated with decreased CO 2 -saturated catalytic capacity and/or for CO 2concentrating mechanisms (CCMs). These changes increase the energy, nitrogen, phosphorus, iron, zinc and manganese cost of producing and operating Rubisco -PCRC, while biosphere oxygenation decreased the availability of nitrogen, phosphorus and iron. The majority of algae today have CCMs; the timing of their origins is unclear. If CCMs evolved in a low-CO 2 episode followed by one or more lengthy high-CO 2 episodes, CCM retention could involve a combination of environmental factors known to favour CCM retention in extant organisms that also occur in a warmer high-CO 2 ocean. More investigations, including studies of genetic adaptation, are needed.

Enhanced biological carbon consumption in a high CO2 ocean

Nature, 2007

The oceans have absorbed nearly half of the fossil-fuel carbon dioxide (CO 2 ) emitted into the atmosphere since pre-industrial times 1 , causing a measurable reduction in seawater pH and carbonate saturation 2 . If CO 2 emissions continue to rise at current rates, upper-ocean pH will decrease to levels lower than have existed for tens of millions of years and, critically, at a rate of change 100 times greater than at any time over this period 3 . Recent studies have shown effects of ocean acidification on a variety of marine life forms, in particular calcifying organisms 4-6 . Consequences at the community to ecosystem level, in contrast, are largely unknown. Here we show that dissolved inorganic carbon consumption of a natural plankton community maintained in mesocosm enclosures at initial CO 2 partial pressures of 350, 700 and 1,050 matm increases with rising CO 2 . The community consumed up to 39% more dissolved inorganic carbon at increased CO 2 partial pressures compared to present levels, whereas nutrient uptake remained the same. The stoichiometry of carbon to nitrogen drawdown increased from 6.0 at low CO 2 to 8.0 at high CO 2 , thus exceeding the Redfield carbon:nitrogen ratio of 6.6 in today's ocean 7 . This excess carbon consumption was associated with higher loss of organic carbon from the upper layer of the stratified mesocosms. If applicable to the natural environment, the observed responses have implications for a variety of marine biological and biogeochemical processes, and underscore the importance of biologically driven feedbacks in the ocean to global change.

Dynamic changes in carbonate chemistry in the microenvironment around single marine phytoplankton cells

Nature Communications, 2018

Photosynthesis by marine diatoms plays a major role in the global carbon cycle, although the precise mechanisms of dissolved inorganic carbon (DIC) uptake remain unclear. A lack of direct measurements of carbonate chemistry at the cell surface has led to uncertainty over the underlying membrane transport processes and the role of external carbonic anhydrase (eCA). Here we identify rapid and substantial photosynthesis-driven increases in pH and [CO32−] primarily due to the activity of eCA at the cell surface of the large diatom Odontella sinensis using direct simultaneous microelectrode measurements of pH and CO32− along with modelling of cell surface inorganic carbonate chemistry. Our results show that eCA acts to maintain cell surface CO2 concentrations, making a major contribution to DIC supply in O. sinensis. Carbonate chemistry at the cell surface is therefore highly dynamic and strongly dependent on cell size, morphology and the carbonate chemistry of the bulk seawater.

CO2-concentrating mechanism in cyanobacterial photosynthesis: Organization, physiological role, and evolutionary origin

2013

Cellular and molecular organization of CO2-concentrating mechanism (CCM) of cyanobacteria is reviewed. Primary processes of uptake, translocation and accumulation of inorganic carbon (Ci) in a cell, as well as concentrating of CO2 near the active site of RuBisCO, are presented as one of the specialized functions of the photoautotrophic cell equipped with the C3-type of photosynthesis. The existence of the ССМ expands our understanding of the photosynthetic Ci assimilation. It implies that the metabolic pathways preceding the involvement of Ci into organic products are the important regulatory elements of light and dark reactions of the cell that maintain its homeostasis and adaptation to CO2 limitation. Here we describe the organization of the CCM in cyanobacteria with a special focus on the CCM of relict halo-and alkaliphilic cyanobacteria of soda lakes. We also assess the role of the CCM at the levels of the organism, the biosphere, and evolution.

Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources

Limnology and Oceanography, 1991

Most of the marine phytoplankton species for which data are available are rate saturated for photosynthesis and probably for growth with inorganic C at normal seawater concentrations; 2 of the 17 species are not saturated. Photosynthesis in these two species can probably be explained by assuming that CO, reaches the site of its reaction with RUBISCO (ribulose bisphosphate carboxylase-oxygenase) by passive diffusion. The kinetics of CO, fixation by intact cells are explicable by RUBISCO kinetics typical of (eucaryotic) algae, and a CO,-saturated in vivo RUBISCO activity not more than twice the in vivo light-and inorganic-C-saturated rate of photosynthesis. For the other species, the high affinity in vivo for inorganic C (and several other attributes) could be explained by postulating active influx of inorganic C yielding a higher concentration of CO, available to RUBISCO during steady state photosynthesis than in the medium. Although such a higher concentration of internal CO, in cells with high affinity for inorganic C is found at low (subseawater) levels of external inorganic C, the situation is more equivocal at normal seawater concentrations. In theory, the occurrence of a CO,-concentrating mechanism rather than passive CO, entry (with consequent glycolate synthesis and metabolism or excretion) could reduce the photon, N, Fe, Mn, and MO costs of growth, but increase the Zn and Se costs. Thus far, data on costs are available only for photons and N; these data generally agree with the predicted lower costs for cells with high affinity for inorganic C. The ecological significance of these attributes is that most marine phytoplankters are not likely to have photosynthetic or growth rates reduced by the measured decreases in inorganic C in productive seawater, drawdown of inorganic C in productive seawater (or increase as atmospheric CO, increases) might alter the competitive balance between cells with low and high affinity for inorganic C, and differences in the effectiveness of use of other resources between cells with high and low affinity could cause differences in the rate and extent of resourcelimited growth for communities dominated by high-affinity or low-affinity cells.

SOURCES OF INORGANIC CARBON FOR PHOTOSYNTHESIS BY THREE SPECIES OF MARINE DIATOM1

Journal of Phycology, 1997

Diatoms are an important functional group of marine phytoplankton because of their role in the fixation of atmospheric carbon dioxide (CO 2 ) and transfer of organic carbon to deep waters. Carbon-concentrating-mechanisms, such as active CO 2 and bicarbonate (HCO ) uptake and carbonic Ϫ 3 anhydrase activity, are believed to be essential to marine photosynthesis, because the main carbon-fixing enzyme, ribulose-1,5-bisphosphate carboxylase-oxygenase, is less than half saturated at normal seawater CO 2 concentrations. On the basis of short-term inorganic 14 C uptake experiments, Tortell et al. (1997; Nature 390: 243-244) recently argued that marine diatoms are capable of HCO uptake. However, as discussed Ϫ 3 herein, the extent of HCO uptake cannot be assessed on the Ϫ 3 basis of these experiments. Using short-term 14 CO 2 -disequilibrium experiments, we show that a clone of the marine diatom Phaeodactylum tricornutum takes up little or no HCO even Ϫ 3 under conditions of severe CO 2 limitation. Predicting the response of the oceans to increased CO 2 concentrations will require, among other things, a careful assessment of the extent to which marine algae take up HCO or CO 2 . Because the Ϫ 3 plasmalemma of microalgae is gas permeable, all phytoplankton exchange CO 2 with the growth medium. Experimental results that are merely consistent with HCO uptake are insuf-Ϫ 3 ficient to prove that HCO uptake is occurring. Our results are Ϫ 3