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Impact of environmental conditions on photosynthesis, growth and carbon allocation strategies of hypersaline species of Dunaliella.
Hypersaline environments pose a number of ecological and metabolic challenges to the
organisms that live in them. Primary producers, such as halotolerant species of the green
microalgal genus Dunaliella, are no exception. In this paper we focus on the problems posed
to the acquisition and metabolism of inorganic nutrients and on the consequences of
exposure to high light and UV radiation. We show that not only does growth in high salinity
environments have repercussions on the flow of carbon into osmolytes such as glycerol, it
also affects speciation of inorganic carbon and the uptake of inorganic ions by the cells. The
strategies that Dunaliella adopt to optimize resource utilization and the interactions among
metabolic pathways are also discussed
Ecological implications of algal CCMs and their regulation
The capacity of algae to express CO2 concentrating mechanisms (CCMs) is regulated by environmental factors. Some of these factors, especially photon flux, can influence the instantaneous activity of a CCM without necessarily affecting gene expression or the capacity of the cell to transport inorganic carbon. Other environmental parameters, especially those causing changes in the availability of CO2 dissolved in the surrounding medium, act at a transcriptional level. In this review, the complex interactions between environmental factors in controlling CCM activity will be discussed, as will the ecological consequences of CCMs as they relate to the growth and ecological performance of algal cells in nature. We also consider the consequences of global climate change for the performance of algae with and without CCMs
Inorganic carbon acquisition by Dunaliella tertiolecta (Chlorophyta) involves external carbonic anhydrase and direct HCO3- utilization insensitive to the anion exchange inhibitor DIDS
A mechanism of bicarbonate uptake with a high sensitivity to the putative anion-exchange inhibitor 4,4h-diisothiocyanostilbene-2,2h- disulphonic acid (DIDS) has been previously reported in green algae. In this study, DIDS inhibited net oxygen evolution by Dunaliella tertiolecta by up to 22%, but internal pH regulation, intracellular CO5 accumulation, carbon fixation and affinity for dissolved inorganic carbon (DIC) in Dunaliella tertiolecta showed low or insignificant sensitivity to DIDS. However, in cells grown and tested at pH 9n5, treatment with DIDS elevated the k3n8(HCO6−), suggesting there may be a minor role for a DIDS-sensitive anion-exchange-type HCO6− transporter in DIC acquisition by D. tertiolecta at high pH. In contrast, significant external carbonic anhydrase (CAext) activity and up to 70% inhibition of DIC-dependent O5 evolution by acetozolamide (AZ) suggest that CAext has an important role in DIC acquisition in D. tertiolecta, in normal seawater conditions and at elevated pH. Furthermore, the rate of DIC-dependent photosynthesis at high pH, in the presence of AZ, was 12 times higher than the calculated uncatalysed rate of CO5 supply from HCO6−. This requires some system for direct HCO6− uptake by D. tertiolecta, which may include a DIDS-insensitive mechanism. The effects of DIDS upon indirect measures of DIC acquisition should be interpreted cautiously as DIDS may have non-specific effects upon whole cell function, and affect ion transport processes not directly related to HCO6− uptake
Insights into the evolution of CCMs from comparisons with other resource acquisition and assimilation processes.
Regarding inorganic carbon as ‘just another’ chemical resource used in the
growth of aquatic photolithotrophs, we ask three questions and then attempt to
answer them. (1) How common are catalysed chemical changes of the resource
outside the cell, and accumulation of the resource inside the cell prior to
assimilation, for the diverse chemical resources used? (2) Do acquisition and
assimilationmeet evolutionary optimality criteriawith respect to the use of other
resources? (3) Are there clues to the evolutionary origin of inorganic carbon
concentrating mechanism (CCMs) in the mechanisms of acquisition of other
resources and vice versa? Evidence considered includes molecular genetic
similarities between CCM components and components of other resource
acquisition mechanisms, and palaeogeochemical evidence on the timing of
restrictions on the availability of the resources such that extracellular transformation
ofmaterials, and their accumulationwithin cells prior to assimilation,
are needed. Provisional answers to the questions are as follows: (1) Many
common chemical resources other than inorganic carbon are subject to
extracellular chemical conversion and/or accumulation prior to assimilation,
e.g. ammonium, nitrate, urea, amino acids, organic and inorganic phosphate
and iron; (2) There is some evidence for optimality of CCMs and of less complex
resource acquisition processes, exemplified by NH4 1 entry and assimilation,
though many more data are needed and (3) There are molecular genetic
similarities between CCM components and transporters for other solutes and
components of respiratory NADH dehydrogenases that are consistent with their
use in CCMs representing a derived evolutionary state. Palaeogeochemical
evidence suggests that CCMs evolved later than did at least some of the
extracellular chemical transformation and/or accumulation mechanisms for
other resources
CO2 concentrating mechanisms in algae: mechanisms, environmental modulation and evolution
The evolution of organisms capable of oxygenic photosynthesis paralleled
a long-term reduction in atmospheric CO2 and the increase in
O2. Consequently, the competition between O2 and CO2 for the active
sites of RUBISCO became more and more restrictive to the rate
of photosynthesis. In coping with this situation, many algae and some
higher plants acquired mechanisms that use energy to increase the CO2
concentrations (CO2 concentrating mechanisms, CCMs) in the proximity
of RUBISCO. A number of CCM variants are now found among
the different groups of algae. Modulating the CCMs may be crucial in
the energetic and nutritional budgets of a cell, and a multitude of environmental
factors can exert regulatory effects on the expression of the
CCM components.We discuss the diversity of CCMs, their evolutionary
origins, and the role of the environment with CCM modulation
Algae lacking carbon concentrating mechanisms
Most of the algae and cyanobacteria that have been critically examined express a carbon-concentrating mechanism (CCM) when grown at, or below, the current atmospheric CO2 concentration. This paper considers algae that appear to lack a CCM. Critical examination of the evidence on which the presence or absence of a CCM is decided shows that more information is frequently needed before the criteria can be fully applied. Examples are the pathways of glycolate metabolism in nongreen algae, and the 13C/12C discrimination shown by form ID Rubisco in vitro. The available evidence suggests that the algae lacking CCMs are some terrestrial green microalgae, some florideophyte freshwater red macroalgae, and a number of florideophyte red macroalgae from the supralittoral, littoral, and sublittoral, and almost all of the freshwater chrysophytes and synurophytes examined. Certain environmental, biochemical, and biophysical factors may permit the occurrence of algae lacking CCMs. The absence of CCMs is presumably the plesiomorphic (i.e., ancestral) condition in cyanobacteria (and algae?).Key words: CO2 diffusion, chrysophyte algae, ecology, evolution, green algae, photos
Effects of different nitrogen sources on C fixation and N assimilation in Scenedesmus sp.
Algal evolution in relation to atmospheric CO2: 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 CO2 assimilation. The high CO2 and (initially) O2-free conditions permitted the use of a Rubisco with a high maximum specific reaction rate. As CO2 decreased and O2 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 CO2 affinity and CO2/O2 selectivity correlated with decreased CO2-saturated catalytic capacity and/or for CO2-concentrating 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-CO2 episode followed by one or more lengthy high-CO2 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-CO2 ocean. More investigations, including studies of genetic adaptation, are needed
Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms
Minimum energy (as photon) costs are predicted for core reactions of photosynthesis, for photorespiratory metabolism in algae lacking CO2 concentrating mechanisms (CCMs) and for various types of CCMs; in algae, with CCMs; allowance was made for leakage of CO2 from the internal pool. These predicted values are just compatible with the minimum measured photon costs of photosynthesis in microalgae and macroalgae lacking or expressing CCMs. More energy-expensive photorespiration, for example for organisms using Rubiscos with lower CO2-O2 selectivity coefficients, would be less readily accommodated within the lowest measured photon costs of photosynthesis by algae lacking CCMs. The same applies to the cases of CCMs with higher energy costs of active transport of protons or inorganic carbon species, or greater allowance for significant leakage from the accumulated intracellular pool of CO2. High energetic efficiency can involve a higher concentration of catalyst to achieve a given rate of reaction, adding to the resource costs of growth. There are no obvious mechanistic interpretations of the occurrence of CCMs algae adapted to low light and low temperatures using the rationales adopted for the occurrence of C4 photosynthesis in terrestrial flowering plants. There is an exception for cyanobacteria with low-selectivity Form IA or IB Rubiscos, and those dinoflagellates with low-selectivity Form II Rubiscos, for which very few natural environments have high enough CO2:O2 ratios to allow photosynthesis in the absence of CCMs
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