The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism (original) (raw)
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Computational and Structural Biotechnology Journal
In cyanobacteria, the CO 2-concentrating mechanism (CCM) is a vital biological process that provides effective photosynthetic CO 2 fixation by elevating the CO 2 level near the active site of Rubisco. This process enables the adaptation of cyanobacteria to various habitats, particularly in CO 2-limited environments. Although CCM of freshwater and marine cyanobacteria are well studied, there is limited information on the CCM of cyanobacteria living under alkaline environments. Here, we aimed to explore the molecular components of CCM in 12 alkaliphilic cyanobacteria through genome-based analysis. These cyanobacteria included 6 moderate alkaliphiles; Pleurocapsa sp. PCC 7327, Synechococcus spp., Cyanobacterium spp., Spirulina subsalsa PCC 9445, and 6 strong alkaliphiles (i.e. Arthrospira spp.). The results showed that both groups belong to β-cyanobacteria based on β-carboxysome shell proteins with form 1B of Rubisco. They also contained standard genes, ccmKLMNO cluster, which is essential for β-carboxysome formation. Most strains did not have the high-affinity Na + /HCO 3 − symporter SbtA and the medium-affinity ATP-dependent HCO 3 − transporter BCT1. Specifically, all strong alkaliphiles appeared to lack BCT1. Beside the transport systems, carboxysomal β-CA, CcaA, was absent in all alkaliphiles, except for three moderate alkaliphiles: Pleurocapsa sp. PCC 7327, Cyanobacterium stranieri PCC 7202, and Spirulina subsalsa PCC 9445. Furthermore, comparative analysis of the CCM components among freshwater, marine, and alkaliphilic β-cyanobacteria revealed that the basic molecular components of the CCM in the alkaliphilic cyanobacteria seemed to share more degrees of similarity with freshwater than marine cyanobacteria. These findings provide a relationship between the CCM components of cyanobacteria and their habitats.
Functional profiling of cyanobacterial genomes and its role in ecological adaptations
Genomics Data, 2016
With the availability of complete genome sequences of many cyanobacterial species, it is becoming feasible to study the broad prospective of the environmental adaptation and the overall changes at transcriptional and translational level in these organisms. In the evolutionary phase, niche-specific competitive forces have resulted in specific features of the cyanobacterial genomes. In this study, functional composition of the 84 different cyanobacterial genomes and their adaptations to different environments was examined by identifying the genomic composition for specific cellular processes, which reflect their genomic functional profile and ecological adaptation. It was identified that among cyanobacterial genomes, metabolic genes have major share over other categories and differentiation of genomic functional profile was observed for the species inhabiting different habitats. The cyanobacteria of freshwater and other habitats accumulate large number of poorly characterized genes. Strain specific functions were also reported in many cyanobacterial members, of which an important feature was the occurrence of phage-related sequences. From this study, it can be speculated that habitat is one of the major factors in giving the shape of functional composition of cyanobacterial genomes towards their ecological adaptations.
α-cyanobacteria possessing form IA RuBisCO globally dominate aquatic habitats
The ISME Journal
RuBisCO (ribulose 1,5-bisphosphate carboxylase/oxygenase) is one the most abundant enzymes on Earth. Virtually all food webs depend on its activity to supply fixed carbon. In aerobic environments, RuBisCO struggles to distinguish efficiently between CO2 and O2. To compensate, organisms have evolved convergent solutions to concentrate CO2 around the active site. The genetic engineering of such inorganic carbon concentrating mechanisms (CCMs) into plants could help facilitate future global food security for humankind. In bacteria, the carboxysome represents one such CCM component, of which two independent forms exist: α and β. Cyanobacteria are important players in the planet’s carbon cycle and the vast majority of the phylum possess a β-carboxysome, including most cyanobacteria used as laboratory models. The exceptions are the exclusively marine Prochlorococcus and Synechococcus that numerically dominate open ocean systems. However, the reason why marine systems favor an α-form is cu...
An Expanded Genomic Representation of the Phylum Cyanobacteria
Genome Biology and Evolution, 2014
Molecular surveys of aphotic habitats have indicated the presence of major uncultured lineages phylogenetically classified as members of the Cyanobacteria. One of these lineages has recently been proposed as a nonphotosynthetic sister phylum to the Cyanobacteria, the Melainabacteria, based on recovery of population genomes from human gut and groundwater samples. Here, we expand the phylogenomic representation of the Melainabacteria through sequencing of six diverse population genomes from gut and bioreactor samples supporting the inference that this lineage is nonphotosynthetic, but not the assertion that they are strictly fermentative. We propose that the Melainabacteria is a class within the phylogenetically defined Cyanobacteria based on robust monophyly and shared ancestral traits with photosynthetic representatives. Our findings are consistent with theories that photosynthesis occurred late in the Cyanobacteria and involved extensive lateral gene transfer and extends the recognized functionality of members of this phylum.
CyanoBase: the cyanobacteria genome database update 2010
Nucleic Acids Research, 2010
CyanoBase (http://genome.kazusa.or.jp/cyanobase) is the genome database for cyanobacteria, which are model organisms for photosynthesis. The database houses cyanobacteria species information, complete genome sequences, genomescale experiment data, gene information, gene annotations and mutant information. In this version, we updated these datasets and improved the navigation and the visual display of the data views. In addition, a web service API now enables users to retrieve the data in various formats with other tools, seamlessly.
2021
Cyanobacteria, the only known photosynthetic prokaryotes, are ancient organisms regarded as the producers of the Earth's oxygenic atmosphere and the ancestors of plant chloroplasts. Contemporary cyanobacteria have evolved as widely-diverse organisms in colonizing most aquatic and soil biotopes, where they face various environmental challenges and competition or symbiosis with other organisms. Cyanobacteria exhibit a wide morphological diversity (unicellular/multicellular, cylindrical/spherical shapes) and many species differentiate specialized cells for growth and survival under adverse conditions. They convert captured solar energy at high efficiencies, to fix an enormous amount of carbon from CO 2 into a huge biomass that sustains a large part of the food chain, and they tolerate high CO 2 content in gas streams. They also synthesize a vast array of biologically active metabolites with great interests for human health and industries. Hence, they are viewed as promising "low-cost" cell factories for the carbon-neutral production of chemicals, thanks to their simple nutritional requirements, their metabolic robustness and plasticity, and the powerful genetics of some model strains. In 2013 when ABR vol 65 entitled "Genomics of Cyanobacteria" was published, approximately 70 cyanobacteria had their genomes fully or partially sequenced. Since then, the number has increased up to about 2000 (https:// genome.jgi.doe.gov/portal/), genome editing studies using CRISPR/Cas have been reported in several model cyanobacteria (Gale et al., 2019; ☆ Footnote: Follow-up of Volume 65: Genomics of Cyanobacteria.
Proceedings of The National Academy of Sciences, 2008
Unicellular cyanobacteria have recently been recognized for their contributions to nitrogen fixation in marine environments, a function previously thought to be filled mainly by filamentous cyanobacteria such as Trichodesmium. To begin a systems level analysis of the physiology of the unicellular N2-fixing microbes, we have sequenced to completion the genome of Cyanothece sp. ATCC 51142, the first such organism. Cyanothece 51142 performs oxygenic photosynthesis and nitrogen fixation, separating these two incompatible processes temporally within the same cell, while concomitantly accumulating metabolic products in inclusion bodies that are later mobilized as part of a robust diurnal cycle. The 5,460,377-bp Cyanothece 51142 genome has a unique arrangement of one large circular chromosome, four small plasmids, and one linear chromosome, the first report of a linear element in the genome of a photosynthetic bacterium. On the 429,701-bp linear chromosome is a cluster of genes for enzymes involved in pyruvate metabolism, suggesting an important role for the linear chromosome in fermentative processes. The annotation of the genome was significantly aided by simultaneous global proteomic studies of this organism. Compared with other nitrogen-fixing cyanobacteria, Cyanothece 51142 contains the largest intact contiguous cluster of nitrogen fixation-related genes. We discuss the implications of such an organization on the regulation of nitrogen fixation. The genome sequence provides important information regarding the ability of Cyanothece 51142 to accomplish metabolic compartmentalization and energy storage, as well as how a unicellular bacterium balances multiple, often incompatible, processes in a single cell. diurnal rhythm ͉ linear chromosome ͉ nitrogen fixation ͉ optical mapping ͉ proteomics
Cyanobacteria: the bright and dark sides of a charming group
Biodiversity and Conservation, 2015
Cyanobacteria are some of the oldest organisms known. Thanks to their photosynthetic apparatus, capable of splitting water into O 2 , protons, and electrons, this large and morphologically diverse group of phototrophic prokaryotes transformed Earth's atmosphere to one suitable for aerobic metabolism and complex life. The long debated Endosymbiotic Theory attributes to cyanobacteria also a significant role in the evolution of life, as important players in plastid origin of higher plants and other photosynthetic eukaryotes. Recent molecular surveys are trying to understand how, exactly, cyanobacteria contributed to plant genome evolution. Their ancient origin and their widespread distribution have recently opened the possibility of including fossil cyanobacterial DNA into the palaeo-reconstructions of various environments and in the calibration of historical records. Cyanobacteria occur in almost every habitat on Earth and can be found in environments subject to stressful conditions, such as desert soils, glaciers, and hot springs. They are common also in urban areas, where they are involved in biodeterioration phenomena. Their great adaptability and versatility are due to a characteristic cell structure, with typical inclusions and particular envelopes. They are the most complex prokaryotes, since they are able to form filaments, colonies, and mats, and they exhibit distinctive ways of movements. To live in different environments, facing biotic and abiotic stresses, cyanobacteria produce also a large array of metabolites, which have potential applications in several fields, such as nutrition, medicine, and agriculture. They have also an important ecological role, not only as primary producers, but also because of their coexistence (often, but not exclusively, in the form of symbiosis) with other organisms to which they supply nitrogen. On the other side, cyanobacteria can have also a negative impact both on the environment and society. In particular they can release a range of toxic compounds, cyanotoxins, diverse in structure and in their effects on human and animal health. In spite of their importance, cyanobacterial identification is not always easy and the use of modern methods (e.g., molecular Communicated by Anurag chaurasia.
Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria
Frontiers in Genetics, 2020
Several cyanobacterial species are dominant primary producers in hot spring microbial mats. To date, hot spring cyanobacterial taxonomy, as well as the evolution of their genomic adaptations to high temperatures, are poorly understood, with genomic information currently available for only a few dominant genera, including Fischerella and Synechococcus. To address this knowledge gap, the present study expands the genomic landscape of hot spring cyanobacteria and traces the phylum-wide genomic consequences of evolution in high temperature environments. From 21 globally distributed hot spring metagenomes, with temperatures between 32 and 75 • C, 57 medium-and high-quality cyanobacterial metagenome-assembled genomes were recovered, representing taxonomic novelty for 1 order, 3 families, 15 genera and 36 species. Comparative genomics of 93 hot spring genomes (including the 57 metagenome-assembled genomes) and 66 non-thermal genomes, showed that the former have smaller genomes and a higher GC content, as well as shorter proteins that are more hydrophilic and basic, when compared to the non-thermal genomes. Additionally, the core accessory orthogroups from the hot spring genomes of some genera had a greater abundance of functional categories, such as inorganic ion metabolism, translation and post-translational modifications. Moreover, hot spring genomes showed increased abundances of inorganic ion transport and amino acid metabolism, as well as less replication and transcription functions in the protein coding sequences. Furthermore, they showed a higher dependence on the CRISPR-Cas defense system against exogenous nucleic acids, and a reduction in secondary metabolism biosynthetic gene clusters. This suggests differences in the cyanobacterial response to environment-specific microbial communities. This phylum-wide study provides new insights into cyanobacterial genomic adaptations to a specific niche where they are dominant, which could be essential to trace bacterial evolution pathways in a warmer world, such as the current global warming scenario.
The cyanobacterial genome core and the origin of photosynthesis
Proceedings of The National Academy of Sciences, 2006
Comparative analysis of 15 complete cyanobacterial genome sequences, including ''near minimal'' genomes of five strains of Prochlorococcus spp., revealed 1,054 protein families [core cyanobacterial clusters of orthologous groups of proteins (core Cy-OGs)] encoded in at least 14 of them. The majority of the core CyOGs are involved in central cellular functions that are shared with other bacteria; 50 core CyOGs are specific for cyanobacteria, whereas 84 are exclusively shared by cyanobacteria and plants and͞or other plastid-carrying eukaryotes, such as diatoms or apicomplexans. The latter group includes 35 families of uncharacterized proteins, which could also be involved in photosynthesis. Only a few components of cyanobacterial photosynthetic machinery are represented in the genomes of the anoxygenic phototrophic bacteria Chlorobium tepidum, Rhodopseudomonas palustris, Chloroflexus aurantiacus, or Heliobacillus mobilis. These observations, coupled with recent geological data on the properties of the ancient phototrophs, suggest that photosynthesis originated in the cyanobacterial lineage under the selective pressures of UV light and depletion of electron donors. We propose that the first phototrophs were anaerobic ancestors of cyanobacteria (''procyanobacteria'') that conducted anoxygenic photosynthesis using a photosystem I-like reaction center, somewhat similar to the heterocysts of modern filamentous cyanobacteria. From procyanobacteria, photosynthesis spread to other phyla by way of lateral gene transfer.