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Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth.

ABSTRACT: We analyzed the metabolic rhythms and differential gene expression in the unicellular, diazotrophic cyanobacterium Cyanothece sp. strain ATCC 51142 under N(2)-fixing conditions after a shift from normal 12-h light-12-h dark cycles to continuous light. We found that the mRNA levels of approximately 10% of the genes in the genome demonstrated circadian behavior during growth in free-running (continuous light) conditions. The genes for N(2) fixation displayed a strong circadian behavior, whereas photosynthesis and respiration genes were not as tightly regulated. One of our main objectives was to determine the strategies used by these cells to perform N(2) fixation under normal day-night conditions, as well as under the greater stress caused by continuous light. We determined that N(2) fixation cycled in continuous light but with a lower N(2) fixation activity. Glycogen degradation, respiration, and photosynthesis were also lower; nonetheless, O(2) evolution was about 50% of the normal peak. We also demonstrated that nifH (encoding the nitrogenase Fe protein), nifB, and nifX were strongly induced in continuous light; this is consistent with the role of these proteins during the assembly of the enzyme complex and suggested that the decreased N(2) fixation activity was due to protein-level regulation or inhibition. Many soluble electron carriers (e.g., ferredoxins), as well as redox carriers (e.g., thioredoxin and glutathione), were strongly induced during N(2) fixation in continuous light. We suggest that these carriers are required to enhance cyclic electron transport and phosphorylation for energy production and to maintain appropriate redox levels in the presence of elevated O(2), respectively.

SUBMITTER: Toepel J

PROVIDER: S-EPMC2395039 | biostudies-literature | 2008 Jun

REPOSITORIES: biostudies-literature

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Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth.

Toepel Jörg J Welsh Eric E Summerfield Tina C TC Pakrasi Himadri B HB Sherman Louis A LA

Journal of bacteriology 20080404 11

We analyzed the metabolic rhythms and differential gene expression in the unicellular, diazotrophic cyanobacterium Cyanothece sp. strain ATCC 51142 under N(2)-fixing conditions after a shift from normal 12-h light-12-h dark cycles to continuous light. We found that the mRNA levels of approximately 10% of the genes in the genome demonstrated circadian behavior during growth in free-running (continuous light) conditions. The genes for N(2) fixation displayed a strong circadian behavior, whereas ph ...[more]

PMID: 18390663

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Project description:BackgroundLife on earth is strongly affected by alternating day and night cycles. Accordingly, many organisms have evolved an internal timekeeping system with a period of approximately 24 hours. Cyanobacteria are the only known prokaryotes with robust rhythms under control of a central clock. Numerous studies have been conducted to elucidate components of the circadian clock and to identify circadian-controlled genes. However, the complex interactions between endogenous circadian rhythms and external cues are currently not well understood, and a direct and mathematical based comparison between light-mediated and circadian-controlled gene expression is still outstanding. Therefore, we combined and analyzed data from two independent microarray experiments, previously performed under alternating light-dark and continuous light conditions in Cyanothece sp. ATCC 51142, and sought to classify light responsive and circadian controlled genes.ResultsFourier Score-based methods together with random permutations and False Discovery Rates were used to identify genes with oscillatory expression patterns, and an angular distance based criterion was applied to recognize transient behaviors in gene expression under constant light conditions. Compared to previously reported mathematical approaches, the combination of these methods also facilitated the detection of modified amplitudes and phase-shifts of gene expression. Our analysis showed that the majority of diurnally regulated genes, essentially those genes that are maximally expressed during the middle of the light and dark period, are in fact light responsive. In contrast, most of the circadian controlled genes are up-regulated during the beginning of the dark or subjective dark, and are greatly enriched for genes associated with energy metabolism. Many of the circadian controlled and light responsive genes are found in gene clusters within the Cyanothece sp. ATCC 51142 genome. Interestingly, in addition to cyclic expression patterns with a period of 24 hours, we also found several genes that oscillate with an ultradian period of 12 hours, a novel finding among cyanobacteria.ConclusionWe demonstrate that a combination of different analytical methods significantly improved the identification of cyclic and transient gene expression in Cyanothece sp. ATCC 51142. Our analyses provide an adaptable and novel analytical tool to study gene expression in a variety of organisms with diurnal, circadian and ultradian behavior.

Project description:BACKGROUND: The over consumption of fossil fuels has led to growing concerns over climate change and global warming. Increasing research activities have been carried out towards alternative viable biofuel sources. Of several different biofuel platforms, cyanobacteria possess great potential, for their ability to accumulate biomass tens of times faster than traditional oilseed crops. The cyanobacterium Cyanothece sp. ATCC 51142 has recently attracted lots of research interest as a model organism for such research. Cyanothece can perform efficiently both photosynthesis and nitrogen fixation within the same cell, and has been recently shown to produce biohydrogen--a byproduct of nitrogen fixation--at very high rates of several folds higher than previously described hydrogen-producing photosynthetic microbes. Since the key enzyme for nitrogen fixation is very sensitive to oxygen produced by photosynthesis, Cyanothece employs a sophisticated temporal separation scheme, where nitrogen fixation occurs at night and photosynthesis at day. At the core of this temporal separation scheme is a robust clocking mechanism, which so far has not been thoroughly studied. Understanding how this circadian clock interacts with and harmonizes global transcription of key cellular processes is one of the keys to realize the inherent potential of this organism. RESULTS: In this paper, we employ several state of the art bioinformatics techniques for studying the core circadian clock in Cyanothece sp. ATCC 51142, and its interactions with other key cellular processes. We employ comparative genomics techniques to map the circadian clock genes and genetic interactions from another cyanobacterial species, namely Synechococcus elongatus PCC 7942, of which the circadian clock has been much more thoroughly investigated. Using time series gene expression data for Cyanothece, we employ gene regulatory network reconstruction techniques to learn this network de novo, and compare the reconstructed network against the interactions currently reported in the literature. Next, we build a computational model of the interactions between the core clock and other cellular processes, and show how this model can predict the behaviour of the system under changing environmental conditions. The constructed models significantly advance our understanding of the Cyanothece circadian clock functional mechanisms.

Project description:Cyanobacteria are oxygenic photosynthetic prokaryotes with important roles in the global carbon and nitrogen cycles. Unicellular nitrogen-fixing cyanobacteria are known to be ubiquitous, contributing to the nitrogen budget in diverse ecosystems. In the unicellular cyanobacterium Cyanothece sp. strain ATCC 51142, carbon assimilation and carbohydrate storage are crucial processes that occur as part of a robust diurnal cycle of photosynthesis and nitrogen fixation. During the light period, cells accumulate fixed carbon in glycogen granules to use as stored energy to power nitrogen fixation in the dark. These processes have not been thoroughly investigated, due to the lack of a genetic modification system in this organism. In bacterial glycogen metabolism, the glgX gene encodes a debranching enzyme that functions in storage polysaccharide catabolism. To probe the consequences of modifying the cycle of glycogen accumulation and subsequent mobilization, we engineered a strain of Cyanothece 51142 in which the glgX gene was genetically disrupted. We found that the ΔglgX strain exhibited a higher growth rate than the wild-type strain and displayed a higher rate of nitrogen fixation. Glycogen accumulated to higher levels at the end of the light period in the ΔglgX strain, compared to the wild-type strain. These data suggest that the larger glycogen pool maintained by the ΔglgX mutant is able to fuel greater growth and nitrogen fixation ability.IMPORTANCE Cyanobacteria are oxygenic photosynthetic bacteria that are found in a wide variety of ecological environments, where they are important contributors to global carbon and nitrogen cycles. Genetic manipulation systems have been developed in a number of cyanobacterial strains, allowing both the interruption of endogenous genes and the introduction of new genes and entire pathways. However, unicellular diazotrophic cyanobacteria have been generally recalcitrant to genetic transformation. These cyanobacteria are becoming important model systems to study diurnally regulated processes. Strains of the Cyanothece genus have been characterized as displaying robust growth and high rates of nitrogen fixation. The significance of our study is in the establishment of a genetic modification system in a unicellular diazotrophic cyanobacterium, the demonstration of the interruption of the glgX gene in Cyanothece sp. strain ATCC 51142, and the characterization of the increased nitrogen-fixing ability of this strain.

Dataset Information

Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth.

Publications

Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth.

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