The genome of
            <i>Cyanothece</i>
            51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle

Welsh, Eric A.; Liberton, Michelle; Stöckel, Jana; Loh, Thomas Kwok Seng; Elvitigala, Thanura R.; Wang, Chunyan; Wollam, Aye; Fulton, Robert S.; Clifton, Sandra W.; Jacobs, Jon; Aurora, Rajeev; Ghosh, Bijoy K.; Sherman, Louis A.; Smith, Richard D.; Wilson, Richard K.; Pakrasi, Himadri B.

doi:10.1073/pnas.0805418105

Cited by 153 publications

(153 citation statements)

References 43 publications

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“…do not have the conventionally defined streamlined genomes seen in other marine taxa (40,42,(45)(46)(47). Similar to IMS101, these genomes are enriched in predicted insertion sequences, repeats, and regulatory proteins (41,48,49), yet despite this fact still retain much larger coding percentages (≥80%) than Trichodesmium. Until now, the low gene density and large intergenic spacers have only been observed in the genome of IMS101 that has been maintained in culture for approximately two decades.…”

Section: Significancementioning

confidence: 86%

“…Accordingly, the IMS101 genome encodes 5,076 proteins (per the IMG annotation https://img.jgi.doe.gov/), yielding a coding percentage of ∼60%, whereas its sympatric, picoplanktonic cousins Prochlorococcus, marine Synechococcus, Crocosphaera watsonii, and Cyanothece (41,48,53,54), and all of the 45 currently sequenced members of the Oscillatoriales (the cyanobacterial order with which IMS101 is phylogenetically placed) have coding percentages >75%. The Oscillatoriales demonstrates variation both in gene count and genome size (average gene number = 5,663.6 ± 1,150.1; average genome size = 6,346,139 ± 1,207,411), and although the number of genes in IMS101 is within this range, the coding percentage and the genome size are at opposite ends of the spectrum, respectively (Dataset S1).…”

Section: Significancementioning

confidence: 99%

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Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Walworth

Pfreundt

Nelson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Understanding the evolution of the free-living, cyanobacterial, diazotroph Trichodesmium is of great importance because of its critical role in oceanic biogeochemistry and primary production. Unlike the other >150 available genomes of free-living cyanobacteria, only 63.8% of the Trichodesmium erythraeum (strain IMS101) genome is predicted to encode protein, which is 20-25% less than the average for other cyanobacteria and nonpathogenic, free-living bacteria. We use distinctive isolates and metagenomic data to show that low coding density observed in IMS101 is a common feature of the Trichodesmium genus, both in culture and in situ. Transcriptome analysis indicates that 86% of the noncoding space is expressed, although the function of these transcripts is unclear. The density of noncoding, possible regulatory elements predicted in Trichodesmium, when normalized per intergenic kilobase, was comparable and twofold higher than that found in the gene-dense genomes of the sympatric cyanobacterial genera Synechococcus and Prochlorococcus, respectively. Conserved Trichodesmium noncoding RNA secondary structures were predicted between most culture and metagenomic sequences, lending support to the structural conservation. Conservation of these intergenic regions in spatiotemporally separated Trichodesmium populations suggests possible genus-wide selection for their maintenance. These large intergenic spacers may have developed during intervals of strong genetic drift caused by periodic blooms of a subset of genotypes, which may have reduced effective population size. Our data suggest that transposition of selfish DNA, low effective population size, and high-fidelity replication allowed the unusual "inflation" of noncoding sequence observed in Trichodesmium despite its oligotrophic lifestyle. marine microbiology | oligotrophic | evolution genomics | nitrogen fixation T he low availability of N (and fixed carbon) in the midlatitude upper oceans provides an important niche for autotrophic organisms that can fix atmospheric nitrogen, which can exert control over global primary production (1-3). Nitrogen fixation is a prokaryotic process with a high-energy demand, and oceanic cyanobacteria are known to be significant sources of this "new" nitrogen (nitrogen that is fixed from the atmosphere or NO 3 advected from depth) (4, 5). Molecular field data have shown that a handful of cyanobacterial diazotrophs responsible for oligotrophic nitrogen fixation can reach relatively high cell numbers (6-12) and be of significant biogeochemical importance (13-16). These include photosynthetic free-living forms, such as the filamentous Trichodesmium and the unicellular Crocosphaera and Cyanothece, and photosynthetic and nonphotosynthetic symbiotic forms, such as heterocystous Richelia and Candidatus Atelocyanobacterium thalassa (3,5,17).Trichodesmium cells can grow either as trichomes (i.e., filaments) or aggregates and form three types of classically described colonies, including radial puffs, vertically aligned fusiform tufts, and bowties (...

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Section: Significancementioning

confidence: 86%

Section: Significancementioning

confidence: 99%

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Walworth

Pfreundt

Nelson

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…In Cyanothece the kai genes exist in multiple copies (12), and the Kai proteins have not been studied in the detail achieved for S. elongatus. The daily modulation of the metabolic activity and gene transcription, namely alternation of photosynthetic and N 2 -fixation phases, has been attributed to the control by the circadian clock largely because the observed period was ∼24 h, even in continuous light following a 12-h light/12-h dark entrainment (13).…”

mentioning

confidence: 99%

Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142

Červený

Sinetova

Valledor

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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The unicellular cyanobacterium Cyanothece sp. American Type Culture Collection (ATCC) 51142 is capable of performing oxygenic photosynthesis during the day and microoxic nitrogen fixation at night. These mutually exclusive processes are possible only by temporal separation by circadian clock or another cellular program. We report identification of a temperature-dependent ultradian metabolic rhythm that controls the alternating oxygenic and microoxic processes of Cyanothece sp. ATCC 51142 under continuous high irradiance and in high CO 2 concentration. During the oxygenic photosynthesis phase, nitrate deficiency limited protein synthesis and CO 2 assimilation was directed toward glycogen synthesis. The carbohydrate accumulation reduced overexcitation of the photosynthetic reactions until a respiration burst initiated a transition to microoxic N 2 fixation. In contrast to the circadian clock, this ultradian period is strongly temperature-dependent: 17 h at 27°C, which continuously decreased to 10 h at 39°C. The cycle was expressed by an oscillatory modulation of net O 2 evolution, CO 2 uptake, pH, fluorescence emission, glycogen content, cell division, and culture optical density. The corresponding ultradian modulation was also observed in the transcription of nitrogenaserelated nifB and nifH genes and in nitrogenase activities. We propose that the control by the newly identified metabolic cycle adds another rhythmic component to the circadian clock that reflects the true metabolic state depending on the actual temperature, irradiance, and CO 2 availability.

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“…ATCC 51142 (Cyanothece 51142), a unicellular diazotrophic cyanobacterium, is able to grow aerobically under nitrogen-fixing conditions and has been recognized as contributing to the marine nitrogen cycle. The recent sequencing of the Cyanothece 51142 genome and its transcriptional analysis have uncovered the diurnally oscillatory metabolism of the bacterium in alternating light-dark cycles (photosynthesis during the day and nitrogen fixation at night) (Stöckel et al, 2008;Toepel et al, 2008;Welsh et al, 2008). In general, cyanobacteria use spatial or temporal separation of oxygen-sensitive nitrogen fixation and oxygen-evolving photosynthesis as a strategy for diazotrophic growth (Benemann & Weare, 1974;Fay, 1992).…”

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Mixotrophic and photoheterotrophic metabolism in Cyanothece sp. ATCC 51142 under continuous light

et al. 2010

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The unicellular diazotrophic cyanobacterium Cyanothece sp. ATCC 51142 (Cyanothece 51142) is able to grow aerobically under nitrogen-fixing conditions with alternating light-dark cycles or continuous illumination. This study investigated the effects of carbon and nitrogen sources on Cyanothece 51142 metabolism via 13 C-assisted metabolite analysis and biochemical measurements. Under continuous light (50 mmol photons m "2 s "1 ) and nitrogen-fixing conditions, we found that glycerol addition promoted aerobic biomass growth (by twofold) and nitrogenasedependent hydrogen production [up to 25 mmol H 2 (mg chlorophyll) "1 h "1 ], but strongly reduced phototrophic CO 2 utilization. Under nitrogen-sufficient conditions, Cyanothece 51142 was able to metabolize glycerol photoheterotrophically, and the activity of light-dependent reactions (e.g. oxygen evolution) was not significantly reduced. In contrast, Synechocystis sp. PCC 6803 showed apparent mixotrophic metabolism under similar growth conditions. Isotopomer analysis also detected that Cyanothece 51142 was able to fix CO 2 via anaplerotic pathways, and to take up glucose and pyruvate for mixotrophic biomass synthesis. INTRODUCTIONRising concerns about global warming due to the greenhouse effect have renewed research focused on the biological capture of CO 2 . Cyanobacteria have versatile metabolic capabilities, which allow them to grow under autotrophic, heterotrophic and mixotrophic conditions (Bottomley & Van Baalen, 1978;Eiler, 2006;Yang et al., 2002). More importantly, some cyanobacteria can capture solar energy to fix nitrogen and generate H 2 , thereby serving as a source of biofertilizer and biofuel, while simultaneously consuming atmospheric CO 2 (Bernat et al., 2009;Dutta et al., 2005;Fay, 1992;Madamwar et al., 2000;Tamagnini et al., 2007;Tuli et al., 1996). Cyanothece sp. ATCC 51142 (Cyanothece 51142), a unicellular diazotrophic cyanobacterium, is able to grow aerobically under nitrogen-fixing conditions and has been recognized as contributing to the marine nitrogen cycle. The recent sequencing of the Cyanothece 51142 genome and its transcriptional analysis have uncovered the diurnally oscillatory metabolism of the bacterium in alternating light-dark cycles (photosynthesis during the day and nitrogen fixation at night) (Stöckel et al., 2008;Toepel et al., 2008;Welsh et al., 2008). In general, cyanobacteria use spatial or temporal separation of oxygen-sensitive nitrogen fixation and oxygen-evolving photosynthesis as a strategy for diazotrophic growth (Benemann & Weare, 1974;Fay, 1992). Interestingly, Cyanothece 51142 demonstrates simultaneous N 2 fixation and O 2 evolution under continuous-light conditions, though it appears to be unicellular (Colon-Lopez et al., 1997;Huang & Chow, 1986). For example, a recent study of the transcriptional and translational regulation of continuously illuminated Cyanothece has revealed a strong synthesis capability for nitrogenase and circadian expression of 10 % of its genes (Toepel et al., 2008). Furthermore, Cyanothece str...

show abstract

The genome of Cyanothece 51142, a unicellular diazotrophic cyanobacterium important in the marine nitrogen cycle

Cited by 153 publications

References 43 publications

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Trichodesmium genome maintains abundant, widespread noncoding DNA in situ, despite oligotrophic lifestyle

Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142

Mixotrophic and photoheterotrophic metabolism in Cyanothece sp. ATCC 51142 under continuous light

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