JXB Advance Access originally published online on October 10, 2005
Journal of Experimental Botany 2006 57(2):249-265; doi:10.1093/jxb/eri286
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Published by Oxford University Press [2005] on behalf of the Society for Experimental Biology.
RESEARCH PAPER |
The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism
1Molecular Plant Physiology Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT, Australia
2ARC Centre of Excellence in Plant Energy Biology, Research School of Biological Sciences, The Australian National University, Canberra, ACT, Australia
* To whom correspondence should be addressed. Fax: +61 2 6125 5075. E-mail: murray.badger{at}anu.edu.au
Received 28 April 2005; Accepted 9 August 2005
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Abstract |
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Top
Abstract
IntroductionCyanobacteria probably exhibit the widest range of diversity in growth habitats of all photosynthetic organisms. They are found in cold and hot, alkaline and acidic, marine, freshwater, saline, terrestrial, and symbiotic environments. In addition to this, they originated on earth at least 2.5 billion years ago and have evolved through periods of dramatic O2 increases, CO2 declines, and temperature changes. One of the key problems they have faced through evolution and in their current environments is the capture of CO2 and its efficient use by Rubisco in photosynthesis. A central response to this challenge has been the development of a CO2 concentrating mechanism (CCM) that can be adapted to various environmental limitations. There are two primary functional elements of this CCM. Firstly, the containment of Rubisco in carboxysome protein microbodies within the cell (the sites of CO2 elevation), and, secondly, the presence of several inorganic carbon (Ci) transporters that deliver
intracellularly. Cyanobacteria show both species adaptation and acclimation of this mechanism. Between species, there are differences in the suites of Ci transporters in each genome, the nature of the carboxysome structures and the functional roles of carbonic anhydrases. Within a species, different CCM activities can be induced depending on the Ci availability in the environment. This acclimation is largely based on the induction of multiple Ci transporters with different affinities and specificities for either CO2 or as substrates. These features are discussed in relation to our current knowledge of the genomic sequences of a diverse array of cyanobacteria and their ecological environments.
Key words:
Carboxysomes, CO2 concentrating mechanism, CO2 transporters, cyanobacteria, transporters, ecological genomics, photosynthesis
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Introduction |
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Of all photosynthetic organisms, cyanobacteria probably inhabit the widest range of ecological habitats. They are found in cold and hot, alkaline and acidic, marine, freshwater, saline, terrestrial, and symbiotic environments. This broad habitat range is due to the fact that they evolved a PSII reaction centre that can extract electrons from water and thus are not limited to environments with other scarcer reduced electron donors, as are other non-oxygenic photosynthetic prokaryotes. In fact, cyanobacteria seem to be able to establish competitive growth in almost any environment that has, at least temporarily, liquid water and sunlight. The diversity and adaptability of cyanobacterial species is also in no small part due to the fact that they have withstood the challenges of evolutionary environmental change. Since their appearance at least 2.5 billion years ago (see Giordano et al., 2005
, for a detailed discussion), the earth has experienced periods of high and low temperatures, high and low CO2, and low and high O2 levels. These temporal and spatial variations have been the driving force for the evolution and acquisition of many genes and physiological properties which have enabled successful growth in the diverse range of environments occupied by cyanobacteria today.
The diverse environments occupied by cyanobacterial species vary dramatically with regard to factors that may limit CO2 fixation. Major challenges to photosynthesis include (i) the restricted diffusion of Ci 
species in water, which is only one ten-thousandth of the value in air; (ii) variability in the levels of Ci and the predominant form of Ci, 
or CO2, which is available for uptake; (iii) wide fluctuations in temperatures and light, and (iv) fluctuations in O2 levels, which can vary from anaerobic to supersaturated through a daily cycle. The significance of these challenges are realized when one considers that the capture of CO2 is finally dependent on the CO2-fixing enzyme Rubisco which has inherent inefficiencies that are exacerbated by many of these extreme environmental conditions. This review focuses on how cyanobacteria have met the challenges posed for photosynthetic CO2 acquisition by the development of a flexible CO2 concentrating mechanism (CCM) and particularly addresses what is known about the genomic diversity of the CCM within cyanobacterial species and how this has evolved to match their habitat requirements.
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Environments inhabited by cyanobacteria |
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Table 1 summarizes the various aquatic and terrestrial environments that are commonly inhabited by cyanobacteria. The environmental characteristics that are typical of these various habitats, with particular reference to factors that may influence CO2 acquisition and fixation by photosynthesis being noted, along with a list of common species.
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Marine planktonic environments
Cyanobacteria are an important component of oceanic, coastal, and estuarine marine phytoplankton communities and contribute significantly to the carbon and nitrogen cycling of these environments (Paerl, 2000
). As much of the world's ocean surface waters are nitrogen-deficient, N2-fixing cyanobacteria can compete well in this environment. In warm waters, the non-heterocystous N2-fixing cyanobacteria Trichodesmium and Crocosphaera are vital components of the global nitrogen cycle through the fixation of new nitrogen (Webb et al., 2001). Single-celled cyanobacteria such as Synechococcus and Prochlorococcus are also common and often dominant in the subsurface waters from 40° S to 40° N where they may account for more than 50% of the photosynthetic biomass (Paerl, 2000; Partensky et al., 1999). These picoplankton forms (<5 µm) generally do not have the capacity to fix N2, but their small size, high surface-to-volume ratios, and ability to grow at a range of light intensities, particularly nutrient-rich deep waters, may ensure their access to nitrogen and other nutrients (Paerl, 2000). Cyanobacteria that periodically dominate oligotrophic waters employ various strategies to improve photosynthesis and nutrient acquisition, including the ability to regulate buoyancy (e.g. Trichodesmium), aggregation in colonies and consortia, and light-harvesting pigment adaptation. In addition to their ability to thrive in oligotrophic waters, many cyanobacteria can exploit more nutrient-rich estuaries and seas, sometimes as persistent nuisance blooms.
In general, marine environments are relatively constant in their pH and inorganic carbon conditions compared with freshwater environments. The Ci levels in open oceans are around 2 mM with a pH of 8.3. The 
ratio is over 100 and thus is the dominant form of Ci. Species growing in coastal and estuarine environments may experience more variable environments with inputs of nutrients and freshwater from the land which may lead to higher growth rates. Under these conditions and particularly in estuaries, it is possible for Ci levels to fall and pH to rise.
Freshwater planktonic environments
Cyanobacteria are common in many freshwater aquatic systems including tropical and temperate lakes, rivers, and estuaries. In general, two major groups of cyanobacteria have been identified, the bloom formers and the non-bloom formers (Oliver and Ganf, 2000; Stockner et al., 2000). The distinguishing feature of the bloom formers is their ability to make gas vacuoles. This allows them to regulate their buoyancy and form persistent assemblages on the surface waters, particularly towards the end of summer. The bloom formers tend to be colonial in nature and vary in form and size, from small filaments to large globular colonies. Many of the filamentous forms such as Anabaena and Aphanizomenon are also heterocyst-forming N2-fixers. The non-bloom formers include both single-celled species, such as Synechococcus, and colony formers such as Aphanothece and Aphanocapsa.
Two major environmental variables drive the seasonal development of cyanobacteria in freshwater bodies during summer, namely the changes in stability and stratification of the water column and declining nutrient availability (Oliver and Ganf, 2000). Over the growing season, stratification increases to a maximum in summer, when the water mixing is insufficient to maintain larger and more dense phytoplankton species in the upper layers. The water column separates into an upper epilimnion, where light is high but nutrients are low, and a dark but nutrient-rich hypolimnion. It is during calm weather in summer and autumn that surface blooms develop, associated with reduced nutrients, high light, and higher temperatures. Non-bloom-forming cyanobacteria are generally capable of growth over a wide range of light intensities and both single-celled and colonial forms have been found at different light levels within the upper euphotic zone. The peak abundance is also found during summer and autumn, and the density tends to be less in the high-light surface layers with higher abundance in the lower levels of the euphotic zone where nutrient levels may also be elevated (Stockner et al., 2000).
In general, freshwater environments are much more variable in their pH, Ci and temperature than their marine counterparts. The pH environment is poorly buffered and the depletion of Ci by photosynthetic activity is accompanied by increases in pH and a corresponding increase on the ratio. Thus, during the progression of summer, the upper layers of the euphotic zone become depleted both in nutrients and Ci and pHs may rise to in excess of pH 9 (Talling, 1985). In surface cyanobacterial blooms, it is also likely that O2 levels will rise within the scum due to photosynthesis.
Microbial mats
Cyanobacteria are often the key organism in microbial mats. They form dense micro-scale communities in which a wide range of microbes and their metabolism may be present (Stal, 2000). A typical property of microbial mats is their laminated or stratified structure in which different groups of organisms occur in particular vertical layers and cyanobacteria are associated with the upper layers receiving sufficient light for photosynthesis. Cyanobacteria are the most successful mat-building organisms due to a number of factors. They are the only oxygenic phototrophic prokaryotes and as such have the capacity for net carbon fixation using only light and water. In addition, they may fix N2 and add to the nutrient status of these communities. Finally, as described below, their ability to adapt to the wide fluctuations in environmental conditions experienced by the mats is of great importance to the survival of these communities.
Cyanobacterial mats or crusts are found in a range of aquatic and terrestrial environments including (i) coastal tidal and sand flats, where large areas are covered by water for only a short period during the tide and where wide fluctuations in water content, salinity, and temperature occur; (ii) hypersaline environments which can occur in shallow and sheltered coastal lagoons with high rates of evaporation and low precipitation, such as the coast of the Red Sea; (iii) thermal hot springs, where the combination of high temperature in combination with H2S or acidic conditions decreases biodiversity. Cyanobacterial mats are most common in hot springs at near neutral or alkaline conditions, and are characterized by temperatures up to 70 °C; (iv) various terrestrial environments ranging from coastal dunes to desert soil and rock surfaces where cyanobacteria may form surface crusts or layers associated with the surface of rocks. Cyanobacteria inhabiting terrestrial environments are able to withstand cyclical desiccation and rehydration, and high surface temperatures.
The microbial mat environments are the most extreme environments in which cyanobacteria are found. In these habitats, cyanobacteria are exposed to low nutrient conditions, variable light, long periods of desiccation, and fluctuating salinity and temperature. Microbial mats of all kinds are characterized by a number of factors that have great impacts on photosynthesis. There is a shallow surface photic zone (1–2 mm) where light is rapidly attenuated. The diffusion of CO2 and O2 is limited allowing O2 to build up during the day to over 1000 µM, Ci levels to be greatly depleted and high pH conditions to be established (Stal, 2000; Ward and Castenholz, 2000). This is coupled with high surface temperatures, all of which may put extreme pressures on CO2 acquisition and photosynthesis.
Symbiotic environments
Cyanobacteria are unique in their capacity to form symbiotic associations with a remarkable range of eukaryotic hosts, including plants, fungi, sponges, and protists (Adams, 2000). In most cases the host benefits from the provision of metabolites that contain both nitrogen and carbon. The benefits to cyanobacteria are less clear, but may include protection from environmental extremes such as high-light intensity and desiccation. Many cyanobacterial symbionts are filamentous, are able to fix N2 in heterocysts, and develop motile hormogonia that serve as the infective agents in many of the symbioses. Their host environments range from small cavities in plants, extracellular layers within a lichen thallus or both inter- and extracellular locations within marine sponges.
The symbiotic photosynthetic environment may be buffered within the host, with the CO2 supply being derived either from host respiration or from the external environment. For aerobic environments, Ci may reach the cyanobacterium predominantly as CO2, depending on the extracellular pH. In addition, the CO2 supply may be limited when thalli or cavities are saturated with water. For marine sponges, the direct supply of from seawater is also a possibility.
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Environmental extremes and their influence on CO2 acquisition |
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The environmental extremes experienced by cyanobacteria have significant influence on the strategies that may need to be developed to achieve efficient CO2 capture during photosynthesis. As a solution to these problems, cyanobacteria have developed a sophisticated CCM which is dependent on a variety of active CO2 and
uptake systems and an internal micro-compartment (carboxysome) where the CO2 level is elevated around the active site of Rubisco (see below for more detailed discussion). Table 2 summarizes the occurrence of environmental extremes in various growth habitats and the predicted impact of these extremes on modes of CO2 acquisition and CCM function. These extremes include:- (i) Temperature extremes, which are found in many cyanobacterial environments. The potential impact of temperatures above 30 °C is primarily through their effect on the kinetic properties of Rubisco (Badger, 1980). Rubisco decreases its affinity for CO2 at higher temperatures and its oxygenase activity is accentuated. Thus, cyanobacteria actively photosynthesizing at elevated temperatures may be expected to require more effective CCM activity, and, conversely, at lower temperatures the intervention of CCM activity may be less critical.
- (ii) Variation in the pH of aquatic medium, particularly in freshwater where the
buffer is important in determining the pH. High pHs are associated with a depletion of inorganic carbon by photosynthesis and mean that becomes a more dominant species. In acidic environments the converse is true, with CO2 being dominant and often being associated with levels of CO2 that are at or above atmospheric equilibrium levels. Variation in the levels of inorganic carbon and the predominance of CO2 and as Ci species will have implications for the development of specific CO2 or uptake systems (see later).
- (iii) Wet and dry conditions, often experienced by cyanobacterial stratified communities. When cyanobacterial mats, crusts, and lichen associations are saturated with water, a high diffusive resistance to Ci and O2 diffusion will be created, and active photosynthesis may create local environments of low Ci and elevated O2 levels. These conditions will favour the development of an effective CCM.
- (iv) High and low light extremes. Generally speaking, high light will be associated with higher rates of photosynthesis and higher CCM activity will be required to secure sufficient Ci.
- (v) Variation in O2 levels, particularly in those environments where there are limitations to gas diffusion and the rate of photosynthesis per unit volume of liquid in high. The impact of this will be through effects on Rubisco oxygenase activity and production and excretion of photorespiratory metabolites such as glycolate. This is probably most extreme in cyanobacterial mat communities where the O2 levels in the top 2–3 mm during the day may reach in excess of 1000 µM (4–5 times atmospheric), pH rises to >9, temperatures increase and Ci levels fall (Stal, 2000
; Ward and Castenholz, 2000). Similar effects may also occur in lichens when they are saturated with liquid water; however, temperatures are likely to be less extreme and this will reduce the impacts of increased O2 levels.
- (vi) Ci availability. Both low and high environments are commonly inhabited by cyanobacteria. Obviously high Ci environments, such as waters high in carbonate or bicarbonate (e.g. marine waters and carbonate lakes), will necessitate a less active CCM. Low Ci environments (e.g. freshwater lakes, cyanobacterial mats) will increase the requirement for a strong and flexible CCM.
- (ii) Variation in the pH of aquatic medium, particularly in freshwater where the
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Evolutionary challenges faced by cyanobacteria |
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The evolution of cyanobacteria over the past 2.5 billion years and the relationship to changes in atmospheric CO2 and O2 levels has been speculated on previously (Badger et al., 2002
; Badger and Price, 2003; Raven, 2003). Past atmospheric CO2 levels, when cyanobacteria first arose, were probably over 100-fold higher than present day conditions. In combination with the prevailing low O2 conditions, ancient cyanobacteria would not have required a CCM to achieve effective photosynthesis. The initial development of a CCM in cyanobacteria would have been triggered by changes in CO2 and O2 that caused CO2 to be a limiting resource for photosynthesis and the Rubisco oxygenase reaction to become a significant problem. Clear records for changes in O2 and CO2 before about 600 million years ago are lacking, but is has been inferred that O2 was near present levels by the beginning of the Phanerozoic (600 million years ago) and CO2 may have been around 15–20 times current atmospheric levels (Berner et al., 2003). Given the properties of current cyanobacterial Rubiscos (Badger et al., 1998), these enzymes should have been able to achieve efficient photosynthesis under these conditions. However, about 400 million years ago there was a large decline in CO2 levels and an almost doubling in the oxygen concentration. These changes would have placed significant pressures on cyanobacterial photosynthesis. It has been argued that this may have been the first evolutionary pressure for the development of CCMs in photosynthetic organisms (Raven, 1997; Badger et al., 2002). However, other views of an earlier evolutionary appearance have also been expressed (Raven, 2003). |
The development of a cyanobacterial CCM |
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In response to the pressures of both evolutionary climate change and cyclical environmental extremes, cyanobacteria have evolved a sophisticated CCM to help acquire CO2 for photosynthesis. They have co-evolved a Rubisco which is adapted to optimal performance under the elevated CO2 conditions produced by this mechanism (Badger et al., 1998
). Thus cyanobacterial Rubiscos have much lower affinities for both CO2 and O2 than other algal or higher plant counterparts, but have much higher turnover rates per unit protein. The CCM allows Rubisco to operate near Vmax and a much smaller investment of nitrogen in Rubisco is required to achieve a particular rate of photosynthesis.
The components of the cyanobacterial CCM are shown in Fig. 1. The CCM primarily consists of a number of active Ci transporters which may transport CO2 or from the external environment and deliver it as to the interior of the cell. In the absence of a cytosolic carbonic anhydrase, the internal pool is able to accumulate well above the external level (Price et al., 1998). The other significant component of the CCM is an internal protein microbody called the carboxysome, which contains the cellular Rubisco. In this compartment the accumulated pool is converted to CO2 through the action of specific carboxysomal carbonic anhydrases and CO2 is elevated due to diffusion restrictions on efflux that are proposed to be present as part of the carboxysome protein shell structure (Kaplan and Reinhold, 1999; Price et al., 1998). Depicted in Fig. 1 are two types of cyanobacterial CCMs, which may be classified according to the nature of the carboxysome structures present in the cell. The 
-cyanobacteria possess a Form 1A type Rubisco and distinct -carboxysomes, while the ß-cyanobacteria have Form 1B Rubisco and ß-carboxysomes (Badger et al., 2002). The carboxysome structure is covered in more detail below. Cyanobacterial CCMs exhibit species diversity, particularly with regard to the suite of Ci transporters that a particular cyanobacterium may possess, with ß-cyanobacteria currently demonstrating a greater array of Ci transport options (see below for more detail).
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The first evolutionary steps towards developing a cyanobacterial CCM may have been quite simple and speculation has previously been suggested (Badger et al., 2002
). In the initial stages of CO2 decline, the first step in the development of a CCM would necessarily have been the evolution of a carboxysome structure for Rubisco. This structure is fundamental to enabling the concentration of CO2 and Ci transporters are ineffectual without it. The evolution of both - and ß-carboxysomes within cyanobacteria is intriguing, and is probably linked to lateral gene transfer between photosynthetic proteobacteria and cyanobacteria (Badger et al., 2002). A carboxysomal carbonic anhydrase would, probably, also have been acquired at this stage as the rate of chemical conversion of to CO2 would have been too slow to support photosynthetic CO2 supply. As CO2 limitation became more severe, the CCM would probably have been improved by the development of a diverse array of both CO2 and uptake systems of varying affinities in order actively to acquire Ci from the surrounding environments. |
The elements of the CCM |
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The carboxysome
Carboxysomes have been found in all cyanobacteria characterized to date and homologous polyhedral bodies are also present in a number of chemoautotrophic bacteria (Cannon et al., 2001
). At the genetic level, carboxysomes from all groups share degrees of similarity although there are distinct differences that separate carboxysomes into two groups based on the form of Rubisco associated with the structure. Carboxysomes containing Form 1A Rubisco form one group while those with Form 1B Rubisco form another (Badger et al., 2002). Phylogenetic analysis of the genomes of these two groups has revealed that there are also distinct differences between their carboxysome genes, prompting Badger et al. (2002) to propose that carboxysomes containing Form 1A Rubisco and those containing Form 1B Rubisco should be termed - and ß-carboxysomes, respectively. Under this scheme, the cyanobacteria fall into two groups; - and ß-cyanobacteria producing - and ß-carboxysomes, respectively. Those with -carboxysomes share carboxysome protein homologies with a number of chemoautotrophic proteobacteria while ß-carboxysomes are, to date, confined to the ß-cyanobacteria (Cannon et al., 2002; Badger and Price, 2003).
An understanding of the protein composition of carboxysomes, and details of their assembly, is essential to determining the structure and function of these microbodies and their role in CCMs. Carboxysomal protein composition has been studied in greatest detail in the -carboxysomes, with many studies concentrated on the chemoautotrophic proteobacterium Halothiobacillus neapolitanus (Cannon et al., 2001, 2002). The polypeptides making up the protein coat of -carboxysomes from H. neapolitanus are coded for by genes of the cso type (csoS1A, csoS1B, csoS1C, csoS2, csoS3, orfA, and orfB) as described by Cannon et al. (2002) while the genes cbbL and cbbS code for Rubisco large and small subunits, respectively (Fig. 1). Together, these genes form a putative carboxysome operon (Cannon et al., 2003). Of the proteins residing in the carboxysomal coat of H. neapolitanus, CsoS3 has recently been characterized as an epsilon-class carbonic anhydrase (So et al., 2004), while the CsoS1 proteins are major constituents of the -carboxysome coat (Cannon and Shively, 1983).
Among the cyanobacteria, little information has yet been gathered to describe the protein composition of either - or ß-carboxysomes. Based on gene content, the -cyanobacteria share all of the carboxysomal proteins so far described from proteobacteria (Badger et al., 2002). However, the molecular information for ß-carboxysomes suggests several unique proteins constitute this type of carboxysome. Unlike -carboxysomes, ß-carboxysome proteins are coded for primarily by a cluster of genes of the ccm type (ccmKLMNO), along with the genes for the large and small subunits of Rubisco (rbcL and rbcS) (Fig. 1). In addition, a carboxysomal CA (CcaA) and sometimes extra CcmK homologues are coded for elsewhere on the genome. Based upon homologies between several - and ß-carboxysomal proteins (namely: CcmK/O and CsoS1; and CcmL and Proteins A/B) it is assumed that these proteins will have common functional and/or structural roles in both carboxysome types (Cannon et al., 2002). Interestingly, however, CcmM and CcmN have no sequence homologues in -carboxysomes and CsoS2 and CsoS3 have no homologues in ß-carboxysomes (Badger et al., 2002; Cannon et al., 2002). Nevertheless, it is suggested that CcmM and CcmN may be functionally similar to CsoS2 and CsoS3 in ß-carboxysomes (Cannon et al., 2002). It is also interesting to note that while CsoS3 has now been characterized as an epsilon-CA (So et al., 2004) and that CcmM has a gamma-CA domain (Ludwig et al., 2000), ß-carboxysomal CA activity is currently attributed to CcaA (Price et al., 1992; Yu et al., 1992; Badger et al., 2002).
The models of CO2 fixation in carboxysomes propose that diffuses through the proteinaceous shell of the carboxysome where carbonic anhydrase inside the structure acts to catalyse the formation of CO2. The CO2 concentration can be elevated within the carboxysome with the aid of some poorly understood diffusion barrier, such as the protein shell, that restricts CO2 diffusion out of the carboxysome. The CO2 pump also plays a critical role in recycling leaked CO2, thereby minimizing CO2 loss from the carboxysome (Price et al., 2002). Further information on the role of carboxysomes in the cyanobacterial CCM can be found in several reviews (Price et al., 1998, 2002; Kaplan and Reinhold, 1999; Cannon et al., 2001).
Carboxysomal carbonic anhydrases
The carboxysomal model, shown in Fig. 1, clearly requires the presence of a carbonic anhydrase to generate CO2 from 
However, the presence of a specific carboxysomal CA enzyme was, until recently, only identified in ß-carboxysomes from a number of ß-cyanobacteria (Fukuzawa et al., 1992; Price et al., 1992; Yu et al., 1992). The emergence of complete genome sequences for a number of - and ß-cyanobacteria has revealed variability in the nature of potential carboxysomal CAs (Table 3). None of the -cyanobacteria sequenced so far has a recognizable carboxysomal CA homologue (CcaA), although a beta-CA (note that nomenclature is not related to and ß terminology used for carboxysomes and cyanobacteria) is present in the -Synechococcus genomes (Table 3). In addition, some of the ß-cyanobacteria appear to contain no identifiable carboxysomal CA homologues. The resolution of this apparent conundrum may lie in the recent discovery that the CsoS3 protein of the shell of -carboxysomes has CA activity (So et al., 2004). CsoS3 is present in all -cyanobacteria (Table 3). This raises the distinct possibility that the gamma-CA N-terminal domain of the CcmM protein of ß-carboxysomes (Ludwig et al., 2000) may also be active as a CA in some species of ß-cyanobacteria, such as Trichodesmium, and Thermosynechococcus. It thus appears as though the nature of CA function within the carboxysomes is quite variable, with both shell-based and soluble activities being possible in different species. The implications of this for function of the carboxysomes are not yet clear.
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An analysis of possible alpha, beta, and gamma carbonic anhydrases (Smith and Ferry, 2000
) in cyanobacterial genomes shows that there is a wide diversity in carbonic anhydrase gene content (Badger et al., 2002; So and Espie, 2005; Table 3). The role of these other carbonic anhydrases in cyanobacterial genomes is unclear. However, some species such as Nostoc and Anabaena species may have a range of beta-CAs other than carboxysomal CA (CcaA) and an alpha-CA (EcaA).
The Ci uptake systems
Experimental evidence thus far indicates that there are at least five distinct modes of active Ci uptake in cyanobacteria. However, since this work is primarily based on common laboratory strains such as Synechococcus PCC7942, Synechocystis PCC6803, and Synechococcus PCC7002, there is scope for the discovery of variants, or new transporters, in cyanobacteria from more extreme habitats. The five Ci uptake systems are explained in more detail in the subsequent sections and in Figs 1 and 2, but, in brief, the systems are: (i) BCT1, an inducible high affinity transporter encoded by the cmpABCD operon and belonging to the traffic ATPase family (Omata et al., 1999); (ii) SbtA, an inducible, high affinity Na+-dependent transporter (Shibata et al., 2002); (iii) BicA, a newly discovered low affinity Na+-dependent transporter belonging to the widespread SulP family (Price et al., 2004); (iv) NDH-14, a constitutive CO2 uptake system based on a specialized NDH-1 complex that appears to be located on the thylakoid membrane (Maeda et al., 2002; Shibata et al., 2001; Price et al., 2002); and (v) NDH-13, a second CO2 uptake system based on a modified NDH-1 complex that is inducible under Ci limitation (Shibata et al., 2001; Maeda et al., 2002).
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The BCT1 HCO3– transporter:
The high affinity
transporter, BCT1, belongs to the ATP binding cassette (ABC) transporter family, also known as traffic ATPases because family members are usually energized by ATP (Higgins, 2001). BCT1 was the first cyanobacterial Ci transporter to be convincingly identified and characterized. To date, BCT1 has been physiologically characterized in just one cyanobacterium, namely Synechococcus PCC7942, although close homologues have been detected in six other species (Table 4). In Synechococcus PCC7942, and other species, BCT1 is encoded by the cmpABCD operon and it is induced under Ci limitation (Omata et al., 1999; McGinn et al., 2003; Woodger et al., 2003). When overexpressed in high CO2-grown cells BCT1 displays a photosynthetic affinity for of around 15 µM, and supports a moderate flux rate (Omata et al., 1999). The cmpABCD operon codes for a multimeric four subunit complex that is strongly induced under conditions of relatively severe Ci limitation (Omata and Ogawa, 1986; Omata et al., 1999; McGinn et al., 2003, 2004; Woodger et al., 2003; Wang et al., 2004) and also under high light stress (Reddy et al., 1989), although the latter condition can also exacerbate a condition of Ci limitation (Woodger et al., 2003; McGinn et al., 2004). BCT1 appears to be the only cyanobacterial example of a primary transporter (uniporter) for This transporter is also closely related to the NRT1 transporter from cyanobacteria, which in turn, acts as a high affinity nitrate/nitrite transporter and is encoded by the nrtABCD operon (Omata et al., 1993; Maeda and Omata, 1997).
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The SbtA HCO3– transporter:
The SbtA transporter was first identified in Synechocystis PCC6803 (Shibata et al., 2002
). In Synechocystis PCC6803, the uptake capacity that was attributable to SbtA was shown to be Na+-dependent, requiring around 1 mM Na+ for half maximal uptake activity (Shibata et al., 2002). This finding was consistent with previous physiological studies suggesting that cyanobacteria might possess a 
symporter driven by the standing electrochemical gradient for Na+ (inwardly directed), in turn, maintained by Na+/H+ antiporter activity (Espie and Kandasamy, 1994); a role for Na+ in pH regulation was also mooted. It has been suggested that NtpJ is involved in Ci uptake in Synechocystis PCC6803, possibly as a primary Na+ extrusion pump (Shibata et al., 2002). It is probable that SbtA is a single subunit transporter (although it may reside in the membrane as a homodimer or homotetramer), but it has not yet been established if this is the case. A gain-of-function approach through overexpression of SbtA is required before this can be concluded with any confidence. The protein has, however, been detected in cytoplasmic membranes isolated from Synechocystis PCC6803 with an apparent complex size of around 160 kDa (Zhang et al., 2004). This might indicate that SbtA exists in the membrane as a tetramer. This proteomic study also confirmed that the abundance of SbtA is dramatically increased under Ci limitation in this species.
The BicA HCO3– transporter:
The BicA transporter is the most recently discovered transporter present in cyanobacteria, and like SbtA, is also Na+-dependent (Price et al., 2004). However, it has no obvious sequence similarity to SbtA. BicA was discovered in the coastal marine cyanobacterium Synechococcus PCC7002, and is interesting because it has a relatively low transport affinity (around 38 µM), but is able to support high photosynthetic flux rates. BicA belongs to a large family of eukaryotic and prokaryotic transporters presently annotated as sulphate transporters or permeases in many bacteria (SulP family). Through the use of gain-of-function experiments in the freshwater cyanobacterium, Synechococcus PCC7942, it was revealed that bicA expression alone is sufficient to confer a Na+-dependent, uptake activity. uptake via BicA required around 1.7 mM Na+ for half-maximal uptake activity and reached saturation in the presence of 20 mM Na+ (Price et al., 2004). Two other BicA transporters were identified and characterized in this manner, including one from the ecologically-important oceanic strain, Synechococcus WH8102 and the other from Synechocystis PCC6803. In this assay system, the three BicA transporters had transport affinities that ranged from 74–353 µM, with the Synechocystis PCC6803 form having the lowest affinity and the WH8102 form having the highest affinity. BicA expression is highly inducible under Ci limitation in Synechococcus PCC7002, but appears also to be present at low levels in cells grown at high CO2 (Price et al., 2004). However, in Synechocystis PCC6803 the BicA gene appears to be constitutively expressed (Price et al., 2004; Wang et al., 2004), whereas in Synechococcus WH8102 the expression characteristics are unknown.
CO2 uptake based on specialized NDH-1 complexes:
Early studies had shown that the NDH-1 dehydrogenase complex is involved in active CO2 uptake by cyanobacteria, potentially via supply of ATP generated by NDH-1 generated cyclic electron flow (Ogawa, 1992). However, within ß-cyanobacteria species, exemplified in genome data from Synechocystis PCC6803, there may be a number of distinct types of NDH-1 complexes with different roles within the cell (Ohkawa et al., 1998; Price et al., 1998). The first evidence that cyanobacteria possess NDH-1 complexes specialized for CO2 uptake came from the observation that the gene cluster ndhF3-ndhD3-chpY is necessary for inducible, high affinity CO2 uptake in Synechococcus PCC7002, but importantly it was also found that re-reduction of P700 (light to dark) was unaffected by mutation of this cluster (Sültemeyer et al., 1997; Klughammer et al., 1999).
The NdhD3/D4 proteins, together with NdhF3/F4 components were proposed as components of two forms of a specialized NDH-1 complex involved in catalysing active CO2 uptake by converting CO2 to within the cell (Ohkawa et al., 2000a, b; Shibata et al., 2001; Maeda et al., 2002). In addition to this, two other genes/proteins are involved in enabling the CO2 uptake activity of the NDH-1 complex, and these are referred to here as chpX and chpY (note that Shibata, Ogawa and colleagues have named these genes as cupB and cupA, while Price and co-workers have used the chpX and chpY nomenclature). It is now clear that the ndhF3/ndhD3/chpY genes code for polypeptides that are part of a high affinity CO2 uptake NDH-13 complex, while the ndhF4/ndhD4/chpX genes code for a NDH-14 complex involved in low affinity CO2 uptake (Shibata et al., 2001; Maeda et al., 2002). Recent proteomic studies have confirmed the presence of NdhF4/NdhD4/ChpY/sll1735 in thylakoid membranes as a sub-complex that is induced under conditions of Ci limitation (Herranen et al., 2004; Prommeenate et al., 2004; Zhang et al., 2004; Battchikova et al., 2005). Curiously, such studies have failed to detect the constitutive NdhF3/NdhD3/ChpX proteins in thylakoids. There is still a possibility that the NDH-13 complex is located on the cytoplasmic membrane. Interestingly, Gloeobacter possesses specific genes for the NDH-13 and NDH-14 complexes (Table 4) but does not possess thylakoid membranes; instead the photosystem machinery is located on the plasma membrane, so NDH-I3 must be able to operate on the plasma membrane, at least in Gloeobacter.
Price et al. (2002) have speculated that the ChpX and ChpY polypeptides may be an integral part of the NDH-1 CO2 uptake complex (NDH-13/4) and involved directly in the conversion of CO2 to Recent proteomic data indicates that the NDH-14 complex is restricted to the thylakoid membrane (Ohkawa et al., 2001) thus linking them directly to the photosynthetic electron transport chain. A model of the operation of such an NDH-13/4 CO2-uptake complex has been proposed, where ChpX and Y are speculated to act as specialized unidirectional carbonic anhydrases, allowing proton abstraction associated with the conversion of CO2 to that is linked to electron flow through the NDH-1 complex (Price et al., 2002).
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Regulation of the CCM by Ci limitation |
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Early studies of the CCM in cyanobacteria showed that its activity varies dramatically depending on the degree of Ci limitation that the cells were exposed to during growth (Kaplan et al., 1980
). Thus cells of model species such as Synechococcus PCC7942 and Synechocystis PCC6803 grown at low Ci (<200 µM pH 8.0) have a high photosynthetic affinity for Ci (K0.5 <20 µM), while those grown at high Ci (>2 mm pH 8.0) have a reduced affinity (K0.5 >200 µM) (McGinn et al., 2003; Woodger et al., 2003). Recent studies have shown that this variation in affinity is almost solely due to the induction of various high and medium affinity transporters (BCT1, SbtA, BicA) and the high affinity CO2 NDH-13 uptake system (McGinn et al., 2003, 2004; Woodger et al., 2003). However, the production of more numerous and smaller carboxysomes in species grown at low Ci has also been noted (McKay et al., 1993). The changes in CCM function which occur during induction of a high affinity state are summarized in Fig. 3.
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Cyanobacteria that induce multiple transporters under Ci limitation appear to utilize pairs of Ci transporters with complementary kinetics for the same Ci species. For instance, there are two
transporters present in Synechococcus PCC7002 (Table 4), the BicA transporter has a relatively low transport affinity of around 38 µM but is able to support a high flux rate. Conversely, the SbtA transporter has a high transport affinity of around 2 µM but possesses a lower flux rate. Under steady-state photosynthetic conditions these two transporters achieve a composite photosynthetic affinity of around 6.5 µM and a high flux rate (Price et al., 2004). Likewise, the two CO2 uptake systems present in Synechococcus PCC7942 have been shown to have contrasting kinetics. The constitutive NDH-14 ChpX-containing system has an initial uptake affinity of 10 µM with a high flux rate, whereas the inducible NDH-13 ChpY-based system has an uptake affinity of around 0.9 µM, but is only able to sustain a relatively low flux rate in isolation. Yet in WT cells, the composite uptake rate for CO2 is around 0.8 µM, with a high flux rate (Maeda et al., 2002). Whether this apparent strategy of employing a high flux/low affinity transporter with a low flux/high affinity transporter is a general rule in freshwater and estuarine cyanobacteria and whether it leads to more efficient Ci uptake remains to be generally established. |
Species diversity in the CCM and the relationship to habitat |
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With the genomic sequence data for at least 18 cyanobacterial species, representing 8
and 10 ß-cyanobacteria (Tables 3, 4, 5), it is now possible to correlate the occurrence of known CCM components in species with their cognate ecological habitats and to assess how CCM properties may have adapted to environmental factors that influence Ci acquisition and CO2 fixation (Table 2). The most striking correlation is that all the -cyanobacteria are open ocean marine species. The reason for this exclusive habitat niche is not clear; however, ß-cyanobacteria are represented in both freshwater and marine environments. They appear able to adapt to a much wider range of ecological environments except perhaps the deep sea oligotrophic environments such as those inhabited by some Prochlorococcus (-cyanobacteria) species.
Carboxysome diversity
The most obvious CCM diversity between cyanobacteria is in the nature of the carboxysomes that they possess. It appears that a majority of the marine cyanobacterial species contain -carboxysomes and that -carboxysomes are found only in marine species. However, it is hard to interpret this observation given the lack of understanding about the physiological differences between the two carboxysome types and the functional attributes they may confer. It is possible that the restriction of -cyanobacteria to marine environments is solely related to the evolutionary origins of this group and their interchange of genes with proteobacterial species. Alternatively, their marine restriction may be related to other evolved characteristics unrelated to any aspect of their CCM function. However, it may also be possible that a physiology based on -carboxysomes imposes limits on the range of environments that can be inhabited. Perhaps -carboxysomes are less effective as CO2 concentrating compartments, and thus restrict effective photosynthesis to regions where inorganic carbon supplies are constant and high (2 mM, pH 8.3), temperatures are cool to moderate, and O2 is not elevated. The absence of -cyanobacteria from estuarine environments where more extreme environmental variation occurs supports this notion.
The presence or absence of a clearly identifiable form of soluble CA associated with carboxysomes is also an interesting variable. Based on work with the ß-carboxysomes of Synechococcus PCC7942 (Price et al., 1992; Yu et al., 1992) and Synechocystis PCC6803 (So and Espie, 1998), carboxysomal beta carbonic anhydrase (CcaA) would appear to be present in six of the ß-cyanobacteria listed in Table 3. The apparent absence of CcaA in Nostoc PCC7120, Thermosynechococcus, Gloeobacter, and Trichodesmium suggests a different mode of carboxysome function. As discussed earlier, the gamma-CA of the CcmM shell protein may fill this role, but this implies variation in the subtle detail of carboxysome function within the ß-carboxysome types, based on the nature of CA function. The consequence of this altered functioning for the habitat distribution of species is unclear and remains to be resolved. While Prochlorococcus species clearly lack a CA apart from the CsoS3 shell protein, the -Synechococcus species all have one beta-CA which is very similar between all species. This CA lacks the carboxyl extension characteristic of the CcaA protein of ß-carboxysomes (data not shown), but the possibility that it may also be associated with -carboxysomes cannot be excluded at present.
Ci transporters
As shown in Table 4, there is considerable variation in the suites of Ci transporters that are found in different cyanobacterial species. The association between suites of Ci transporters and species habitat is discussed below.
Marine environments:
The BCT1 transporter is only present in freshwater ß-cyanobacteria and conversely marine cyanobacteria do not possess the BCT1 transporter (or the related NRT1 nitrate transporter: data not shown). The reasons for the absence of BCT1 in marine cyanobacteria are unclear. It may be related to a potential strategy of employing the electrochemical driving force that is associated with maintaining a mandatory standing Na+ gradient (inwardly directed) for energization of Ci uptake, rather than using ATP as a direct energy source for pumping (Bryant, 2003). It is also possible that, in marine environments, where levels are relatively high, there may be a reduced requirement for a high affinity and energy expensive transport system.
The SbtA transporter has a variable representation. Among the ß-cyanobacteria, Synechococcus PCC7002 and Crocosphaera watsonii have strong homologues while Trichodesmium erythraeum lacks it. For the -cyanobacteria, all Prochlorococcus species have a weak homologue (which is not yet proven as a transporter) while of the Synechococcus species only CC9311 has this same weak homologue. The SbtA transporter characterized in ß-cyanobacteria has a relatively high affinity for (Shibata et al., 2002; Price et al., 2004) and may be expected to be present where species are required to grow at significantly reduced Ci. This may be the case for Synechococcus PCC7002 which grows at high temperatures on estuarine mud flats. The presence of SbtA in both Synechococcus PCC7002 and Crocosphaera appears to be correlated with the presence of both low and high affinity CO2 uptake systems, which may indicate that both these species require a full suite of Ci transport options to respond to the Ci environments which they experience. Crocosphaera watsonii is an oligotrophic warm ocean species and should not experience the same extremes as PCC7002, however, aspects of growth in warm, high-light, and nutrient-depleted waters may exert certain stresses that favour the development of a fully flexible CCM. The absence of SbtA from Trichodesmium is correlated with the absence of a high affinity CO2 uptake system (NDH-13), and indicates a clear difference between these two marine nitrogen-fixing species.
The BicA transporter family appears to be the most widely distributed Ci transport system, although the functionality of all the homologues as transporters has not yet been established (Price et al., 2004). For the ß-cyanobacteria, all three marine species have at least one strong homologue and at least one other moderate homologue. Crocosphaera has two strong homologues. For the -cyanobacteria, all Synechococcus species have a strong and a medium homologue, while the Prochlorococcus species only have medium and weak homologues. The BicA transporter would appear to be a medium affinity transporter that can sustain high flux rates of uptake and has been shown to be inducible in Synechococcus PCC7002 (Price et al., 2004) although in Synechococcus WH8102 it may have a lower flux rate. In the absence of other known transporters, BicA transporters in -cyanobacteria may sustain the bulk of the uptake occurring in the marine environment and may be inducible in response to environmental conditions.
The two CO2 uptake systems, NDH-13/4, are most variably represented in the marine cyanobacteria. For the ß-cyanobacteria, the low-affinity uptake system (NDH-14) is present in all three species, while the high-affinity system (NDH-13) is only present in Synechococcus PCC7002 and Crocosphaera (although the genome information is not completely clear for Crocosphaera). For the -cyanobacteria there is considerable variation. The low affinity system is present in the Synechococcus species, while Prochlorococcus species appear to lack any CO2 uptake system.
Freshwater environments:
The BCT1 transporter is present in cyanobacteria from all freshwater environments. It is inducible at low Ci levels in Synechococcus PCC7942 and Synechocystis PCC6803 and would appear to be necessary in all environments where high-affinity uptake of is required. However, the presence of the other two transport systems is more variable. Single strong homologues of the SbtA transporter are present in all the species except Nostoc punctiforme. Interestingly, a weak SbtA homologue closely related to the Prochlorococcus protein is found in the three Nostoc/Anabaena species. BicA is also variable in its presence. Synechocystis PCC6803 and Nostoc PCC7120 have strong and medium homologues, Anabaena variabilis a single strong homologue, while Synechococcus PCC7942 and Nostoc punctiforme have only weak homologues. High and low affinity CO2 uptake systems are present in all species.
Freshwater cyanobacteria have a diverse array of Ci uptake systems. Species such as Synechocystis, Nostoc PCC7120, and Anabaena variabilis may have 5–6 separate and CO2 transport systems which presumably are regulated in their induction to match the external conditions of Ci, pH, O2, and temperature. Other species such as Synechococcus PCC7942 and Nostoc punctiforme lack one or more uptake systems. It would appear that the core transport systems for the operation of the CCM in a freshwater environment are the two CO2 uptake systems and BCT1. Depending on the species, this core is supplemented with other transport systems, presumably to meet specific demands of the environment. It is not surprising that Nostoc PCC7120 has a full suite of Ci transporters as it forms gas vacuoles and would exist in high-light, low-Ci, and low-nutrient waters. The apparent paucity of Ci transporters in Nostoc punctiforme may be related to its symbiotic nature. Although found in free-living forms, its existence in symbiotic associations with cycads may require much less extreme adjustment to environmental variation. The two CO2 uptake systems and the BCT1 transporter may be sufficient in this habitat.
Other environments:
Of the species in Tables 4 and 5, Gloeobacter violaceus and Thermosynechococcus elongatus occupy the most different habitats. Gloeobacter originates from calcareous rock surface environments, while Thermosynechococcus is from thermal hot springs. The consequences of these environments for the Ci transporter complement are interesting. Gloeobacter contains only the two CO2 uptake systems and the BCT1 transporter. The surface of a calcareous rock is presumably more constant in its Ci supply, both as CO2 from the atmosphere and from the underlying rock. In addition, this is a slow-growing species and photosynthesis would require low Ci flux rates. It is unclear in this case if there would be environmental variation in Ci availability that would require the induction of the high-affinity CO2 uptake system and the BCT1 transporter, or if their expression may be more constitutive.
By contrast, one would expect hot springs to be quite an extreme environment for efficient photosynthesis, with its elevated temperatures. However, Thermosynechococcus displays a reduced set of transporters compared with freshwater species. Again, two CO2 uptake systems, the BCT1 transporter and a single medium homologue of the BicA transporter are present. The chemistry of the Beppu hot springs is variable with waters varying from alkaline to acidic. The alkaline waters are dominated by and species from these environments may be subjected to fairly constant levels of CO2 and Under these conditions, great flexibility in varying Ci transporter composition may not be necessary. However, there is variation in the pH and conditions between different thermal pools of this system and widely distributed cyanobacterial species may require flexibility in Ci acquisition strategies. In addition, mat-forming species which inhabit the edges of the pools may experience extremes of Ci and O2 during the day, depending on submersion levels and some flexibility in Ci acquisition strategies between free-living and mat community conditions may also be necessary.
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Conclusions |
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Over the last ten years a detailed understanding of the genes and proteins involved in the formation of a cyanobacterial CCM has emerged. These proteins are involved in two primary aspects of CCM function. Firstly, they are involved in the formation of functional carboxysome microbodies within the cell, where CO2 can be elevated around Rubisco. Secondly, they comprise an array of at least five Ci transport mechanisms, which facilitate flexibility in Ci in diverse environments. During the last five years, genome sequences for at least 18 cyanobacterial species from a range of ecological environments have become available and this has allowed us to view the ecological adaptation of the cyanobacterial CCM from a genomic perspective.
Two types of carboxysomes are found in cyanobacteria and their distribution seems to be correlated with the restriction of some species to oligotrophic open ocean environments where they are often the dominant cyanobacterial species. These are the -cyanobacteria (with -carboxysomes) which include Prochlorococcus and -Synechococcus species. The ß-cyanobacteria (with ß-carboxysomes) are much more widespread, occupying both freshwater and marine environments with a greater range of environmental extremes. Combined with carboxysome diversity, there has been evolution of the nature of carbonic anhydrases which are involved in CO2 generation within the carboxysome. There are at least four classes of CA enzymes represented in cyanobacterial genomes, with a potential for members of at least three of these to be directly involved in carboxysome function (CcaA, CcmM, and CsoS3)
The suites of Ci transporters which are present are also highly variable and perhaps the most highly correlated with nature of the aquatic habitat. Higher affinity Ci transporters are induced under environmental conditions when Ci acquisition for photosynthesis becomes limiting. Open ocean marine species show a restricted complement of transporters, with the extreme represented by Prochlorococcus species which have a limited range of transporters and no CO2 uptake systems. Variable representation of and CO2 uptake systems occurs in other marine species. In general, the maximum complement is present in species which probably experience the most variable environments such as coastal or estuarine environments with fluctuations in Ci levels and temperature. Freshwater species also show a range of Ci transporters. Species which occupy lake environments and peak in their abundance during summer contain the most complete complement of transporters, being correlated with the most extreme environmental fluctuations in Ci, temperature, O2, and nutrients. Species with reduced sets of transporters are correlated with growth in symbiotic environments, thermal hotsprings and calcareous rock, where environmental fluctuations may be much less extreme.
Several more cyanobacterial species are currently being sequenced and sequence information will become available over the next year or so. This will expand the species representation from various environments, particularly marine symbiotic systems (Prochloron and Prochlorothrix species) and more freshwater species such as Microsytis aeruginosa. However, the ability accurately to interpret the presence of genes and their meaning in terms of ecological performance is still limited by a lack of comparative physiology of the CCM in a wide range of cyanobacterial species. Knowledge to date is largely based on three model species, Synechocystis PCC6803, Synechococcus PCC7942, and Synechococcus PCC7004 and interpretation of function in other species is based on this. Hopefully research in the next few years will discover more about the detailed structure and function of carboxysomes and Ci transporters in wider range of cyanobacterial species, allowing the interpretation of genetic diversity of the CCM in relation to the ecological habitat to be improved.
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