The Cyanobacteria: Molecular Biology, Genomics and Evolution
Cyanobacteria and Earth History
The biochemical capacity to use water as the source for electrons in photosynthesis evolved once, in a common ancestor of extant cyanobacteria. The geological record indicates that this transforming event took place early in our planet's history, at least 2450-2320 million years ago (Ma), and possibly much earlier. Geobiological interpretation of Archean (>2500 Ma) sedimentary rocks remains a challenge; available evidence indicates that life existed 3500 Ma, but the question of when oxygenic photosynthesis evolved continues to engender debate and research. A clear paleontological window on cyanobacterial evolution opened about 2000 Ma, revealing an already diverse biota of blue-greens. Cyanobacteria remained principal primary producers throughout the Proterozoic Eon (2500-543 Ma), in part because the redox structure of the oceans favored photautotrophs capable of nitrogen fixation. Green algae joined blue-greens as major primary producers on continental shelves near the end of the Proterozoic, but only with the Mesozoic (251-65 Ma) radiations of dinoflagellates, coccolithophorids, and diatoms did primary production in marine shelf waters take modern form. Cyanobacteria remain critical to marine ecosystems as primary producers in oceanic gyres, as agents of biological nitrogen fixation, and, in modified form, as the plastids of marine algae.
Insights into Cyanobacterial Evolution from Comparative Genomics
Recent high-throughput sequencing has provided DNA sequences at an unprecedented rate, posing considerable analytical challenges, but also offering insight into the genetic mechanisms of adaptation. Here we present a comparative genomics-based approach towards understanding the evolution of these mechanisms in cyanobacteria. Historically, systematic methods of defining morphological traits in cyanobacteria have posed a major barrier in reconstructing their true evolutionary history. The advent of protein, then DNA, sequencing - most notably the use of 16S rRNA as a molecular marker - helped circumvent this barrier and now forms the basis of our understanding of the history of life on Earth. However, these tools have proved insufficient for resolving relationships between closely related cyanobacterial species. The 24 cyanobacteria whose genomes have been compared occupy a wide variety of environmental niches and play major roles in global carbon and nitrogen cycles. By integrating phylogenetic data inferred for hundreds to nearly 1000 protein coding genes common to all or most cyanobacteria, we are able to reconstruct an evolutionary history of the entire phylum, establishing a framework for resolving how their metabolic and phenotypic diversity came about.
Gene transfer to Cyanobacteria in the Laboratory and in Nature
Horizontal (lateral) gene transfer is a postulated mechanism influencing bacterial evolution. Known mechanisms of DNA transfer into cyanobacteria include genetic transformation and conjugation with Escherichia coli, which are widely used in the laboratory with several different cyanobacterial strains. Additionally, direct (likely conjugal) transfer of DNA between cyanobacterial strains has been demonstrated. These transfer mechanisms can represent the basis for genetic recombination in natural populations of cyanobacteria, for which several possible examples have been described, as well as for the horizontal transfer that is deduced for some genes in protein phylogeny studies, which have been made possible by the current availability of numerous complete cyanobacterial genomic sequences.
Molecular Ecology and Environmental Genomics of Cyanobacteria
The application of molecular biology and genomics to microbial ecology has been a transformative force, making possible the discovery of layer upon layer of complexity in natural communities of microbes. Diversity surveying, community fingerprinting, and functional interrogation of natural populations have become common, enabled by a battery of molecular and bioinformatics techniques, some specifically developed for the cyanobacteria. The ensuing effects on our views of cyanobacterial ecology have been perhaps less revolutionary, because of the special characteristics of cyanobacteria among microbes, but also significant. We have come to realize that the present taxonomic system is often phylogenetically incorrect; several new cyanobacteria or groups thereof have been discovered, and some established groups have been found to be constructs. Surveying efforts have covered many habitats and have demonstrated that cyanobacterial communities tend to be habitat-specific, and that plenty of undescribed genetic diversity is concealed among morphologically simple types. We can now select among isolates those that are good representatives of natural populations, enabling, among other objectives, ecologically motivated genome sequencing efforts. We have witnessed the first studies addressing population genetics and the blooming of functional studies based on detection of gene expression in Nature. We are entering an era of expansion of the polyphasic approaches that combine molecular, bioinformatics, physiological, and geochemical techniques to study natural communities
Comparative Genomics of Marine Cyanobacteria and their Phages
At present there are 24 cyanobacteria for which a total genome sequence is available. 15 of these cyanobacteria come from the marine environment. These are six Prochlorococcus strains, seven marine Synechococcus strains, Trichodesmium erythraeum IMS101 and Crocosphaera watsonii WH8501. Several studies have demonstrated how these sequences could be used very successfully to infer important ecological and physiological characteristics of marine cyanobacteria. However, there are many more genome projects currently in progress, amongst those there are further Prochlorococcus and marine Synechococcus isolates, Acaryochloris and Prochloron, the N2-fixing filamentous cyanobacteria Nodularia spumigena, Lyngbya aestuarii and Lyngbya majuscula, as well as bacteriophages infecting marine cyanobaceria. Thus, the growing body of genome information can also be tapped in a more general way to address global problems by applying a comparative approach. Some new and exciting examples of progress in this field are the identification of genes for regulatory RNAs, insights into the evolutionary origin of photosynthesis, or estimation of the contribution of horizontal gene transfer to the genomes that have been analyzed.
Stress Responses in Synechocystis: Regulated Genes and Regulatory Systems
Genome-wide investigations of gene expression at the transcriptional level in cyanobacteria, using DNA microarrays, have allowed identification of genes whose expression is induced or repressed by various types of environmental stress and also of previously uncharacterized genes that appear to be involved in stress responses. Acclimation to stress begins with perception of stress and transduction of the stress signal. A combination of the systematic mutation of potential sensors and transducers and DNA microarray analysis has led to significant progress in understanding the mechanisms of perception of and reaction to environmental stress in cyanobacteria. Recent progress has been made in the identification of stress-inducible genes and of systems that regulate responses to stress that has been made using DNA microarrays in cyanobacteria and, in particular, in Synechocystis sp. PCC 6803.
Bioactive Compounds Produced by Cyanobacteria
Cyanobacteria produce a large variety of bioactive compounds, including substances with anti-cancer and anti-viral activity, UV protectants, specific inhibitors of enzymes, and potent hepatotoxins and neurotoxins. Only a few biosynthetic pathways have been elucidated. So far genes have been identified for several bioactive proteins, "ribosomal" and "non-ribosomal" peptides, and peptide-polyketide hybrid molecules. Potential functions of bioactive compounds for the producing cells and evolutionary aspects are discussed, and methods for the detection of cyanobacterial toxins and harmful cyanobacteria are described.
The Cyanobacterial Circadian Clock and the KaiC Phosphorylation Cycle
The circadian clock is an endogenous timing mechanism in living organisms that coordinates their lives with environmental changes. Cyanobacteria are the simplest organisms that are known to exhibit circadian rhythms, and they have become one of the most successful model organisms for circadian biology. Although the circadian clock in cyanobacteria has the same fundamental features as that in eukaryotes, its individual components that have been identified to date are unique. The molecular mechanism of the cyanobacterial clock is different from that described for the eukaryotic clock. The clock core in cyanobacteria is the KaiC phosphorylation cycle.
Molecular Structure of the Photosynthetic Apparatus
The process of conversion of light energy from the sun into chemical energy is catalyzed by oxygenic photosynthesis. It is the process that provides all higher life on earth with energy. All oxygen in the atmosphere is evolved by this process, which was invented 2.8 billion years ago by the ancestors of cyanobacteria. Cyanobacteria are even nowadays very important members of the global ecosystem, and contribute up to 30% of the yearly oxygen production on earth. The structure and function of the protein complexes that catalyze the first steps of the energy conversion have been described. Light is captured by antenna complexes and transferred to two large bio-solar systems, photosystem I and II, which catalyze the transmembrane charge separation. This drives the photosynthetic process and provides the energy for production of the high-energy substrate ATP and reduced hydrogen in the form of NADPH. The photosystems are functionally coupled by the cytochrome b6f complex, the membrane intrinsic plastoquinone pool and lumenal electron carriers. The reactions of the electron transport chain lead to an electrochemical proton gradient, which drives synthesis of ATP by the molecular motor, the ATP synthase. The structures of the complexes have been described in respect to the function and evolution of the photosynthetic apparatus.
Membrane Systems in Cyanobacteria
Cyanobacteria are photosynthetic prokaryotes with highly differentiated membrane systems. In addition to a Gram-negative-type cell envelope with plasma membrane and outer membrane separated by a periplasmic space, cyanobacteria have an internal system of thylakoid membranes where the fully functional electron transfer chains of photosynthesis and respiration reside. The presence of different membrane systems lends these cells a unique complexity among bacteria. Cyanobacteria must be able to reorganize the membranes, synthesize new membrane lipids, and properly target proteins to the correct membrane system. The outer membrane, plasma membrane, and thylakoid membranes each have specialized roles in the cyanobacterial cell. Understanding the organization, functionality, protein composition and dynamics of the membrane systems remains a great challenge in cyanobacterial cell biology.
Biogenesis and Dynamics of Thylakoid Membranes and the Photosynthetic Apparatus
Thylakoid membranes are the site of the light-reactions of photosynthesis, and they are crucial to the photosynthetic lifestyle of cyanobacteria. Recent knowledge has been obtained regarding the structure, organisation and biogenesis of thylakoid membranes in cyanobacteria. In particular the dynamics of the membrane, and the roles that protein diffusion may play in membrane biogenesis, regulation of photosynthesis and the turnover and repair of the photosynthetic apparatus. Although we have detailed knowledge of many thylakoid membrane components and some thylakoid membrane processes, much remains to be learned about the large-scale organisation and biogenesis of thylakoid membranes.
Carbon Acquisition by Cyanobacteria: Mechanisms, Comparative Genomics and Evolution
Tthe mechanisms of inorganic carbon uptake, photorespiration, and the regulation between the metabolic fluxes involved in photoautotrophic, photomixotrophic and heterotrophic growth have been identified including the genes involved, their regulation and phylogeny.
Nitrogen Assimilation and C/N Balance Sensing
Cyanobacteria inhabit nearly all illuminated environments on Earth and play key roles in the carbon and nitrogen cycle of the biosphere. Generally, cyanobacteria are able to utilize a variety of inorganic and organic sources of combined nitrogen, like nitrate, nitrite, ammonium, urea or some amino acids. Several cyanobacterial strains are also capable of diazotrophic growth. Genome sequencing has provided a large amount of information on the genetic basis of nitrogen metabolism and its control in different cyanobacteria. Comparative genomics, together with functional studies, has led to a significant advance in this field over the past years. 2-oxoglutarate has turned out to be the central signalling molecule reflecting the carbon/nitrogen balance of cyanobacteria. Central players of nitrogen control are the global transcriptional factor NtcA, which controls the expression of many genes involved in nitrogen metabolism, as well as the PII signalling protein, which fine-tunes cellular activities in response to changing C/N conditions. These two proteins are sensors of the cellular 2-oxoglutarate level and have been conserved in all cyanobacteria. In contrast, the adaptation to nitrogen starvation involves heterogeneous responses in different strains.
Transcriptional and Developmental Responses by Anabaena to Deprivation of Fixed Nitrogen
Deprivation of fixed nitrogen, to which the formation of dinitrogen-fixing cells called heterocysts is a conspicuous response, appears to initiate a switch from reliance on photosynthesis for ATP, reductant, and carbon to reliance-in developing cells-on endogenous glycogen stores, heightened utilization of the oxidative pentose phosphate pathway, and-at least in mature heterocysts-photosystem I and influx from vegetative cells. Sugars are needed to produce heterocyst envelope layers of polysaccharide and glycolipid. Decreased transcription and translation of a few highly expressed genes may make possible the increased transcription and translation of many others. Although we interpret metabolic capabilities from microarray data, we stress the hazards of doing so, and emphasize that the interpretations remain to be evaluated. Little is known of the regulation of gene expression during heterocyst differentiation. NtcA is required for the expression of nrrA and many other genes, NrrA is required for the full induction of hetR, and HetR is required for the expression of many downstream genes. Numerous regulatory-family genes are significantly induced during heterocyst differentiation and may importantly regulate the process. Some genes of unknown function increase many-fold in expression during differentiation, leading one to wonder what their roles may be.
Cyanobacterial Nitrogen Fixation in the Ocean: Diversity, Regulation and Ecology
Nitrogen is an essential and major component of biomass. While virtually all life depends on combined forms of nitrogen that are usually limited in availability, some prokaryotes, including many groups of cyanobacteria, can use the ubiquitous atmospheric dinitrogen (N2). As photoautotrophic bacteria they can easily meet the energy demand that is required by nitrogenase, the enzyme that reduces N2to NH3. However, nitrogenase is very sensitive to oxygen and the oxygenic cyanobacteria have evolved various strategies to cope with this paradox. Primary production in the ocean is generally considered to be limited by nitrogen. In recent years it has become clear that N2-fixing cyanobacteria are important in the nitrogen budget of the surface oceans. Estimates of N2 fixation indicate that approximately half of global N2 fixation occurs in the sea. N2 fixation is not distributed homogenously throughout the oceans. Pelagic diazotrophic cyanobacteria are only found in (sub)tropical oceans and are notably absent in temperate and colder seas. However, at lower salinities in estuaries and other brackish environments, N2-fixing cyanobacteria can be abundant. N2-fixing cyanobacteria are also abundant in benthic mats in coastal and aquatic environments all over the globe, including polar regions. This demonstrates that N2-fixing cyanobacteria are not excluded from temperate and cold marine environments, even though they are only found in the water column of warm oceans.
Cyanobacterial-plant Symbioses: Signalling and Development
Cyanobacteria form stable nitrogen-fixing symbioses with diverse eukaryotes. With few exceptions the cyanobacteria belong to the terrestrial and widespread genus Nostoc. This genus has a notable morphological plasticity which may be in part responsible for its symbiotic competence. In contrast, the symbiotic host range is wide, from mosses to angiosperms. The plant symbioses range from less intimate interactions, such as in mosses, to highly intricate symbioses, such as the intracellular symbiosis with the angiosperm Gunnera. In Azolla spp. the relationship is perpetual and maintained between generations. Nostoc is also one of the most developmentally advanced prokaryotes and capable of differentiating several cell types with various functions. Individual vegetative cells of Nostoc may differentiate into nitrogen-fixing heterocysts, and filaments may fragment into hormogonia, a motile life-stage and a prerequisite for plant infection. On internalization, the hormogonia are turned into multi-heterocystous filaments. The high frequency of heterocysts is reflected in their high nitrogen-fixing activities, and in the transfer of the fixed nitrogen to the plant. A sequence of inter-organism communication events between the partners and cellular adaptations is therefore obvious.
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