Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera

Fu, Fei-Xue; Mulholland, Margaret R.; Garcia, Nathan S.; Beck, Aaron J.; Bernhardt, Peter; Warner, Mark E.; Sañudo‐Wilhelmy, Sergio A.; Hutchins, David A.

doi:10.4319/lo.2008.53.6.2472

Cited by 145 publications

(161 citation statements)

References 55 publications

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“…It is widely distributed in tropical and subtropical waters (reported from the North and South Atlantic Ocean, North and South Pacific Ocean and the Arabian Sea), but reports on its physiology or ecology are still very recent (Falcó n et al, 2004(Falcó n et al, , 2005Tuit et al, 2004;Dyhrman and Haley, 2006;Zehr et al, 2007a;Fu et al, 2008;Compaoré and Stal, 2009;Hewson et al, 2009;Webb et al, 2009). The draft genome of C. watsonii WH 8501 is 6.24 Mb, with 323 contigs encoding a total of 5958 candidate protein-encoding genes (http://microbes.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

et al. 2010

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The unicellular cyanobacterium Crocosphaera watsonii is an important nitrogen fixer in oligotrophic tropical and subtropical oceans. Metabolic, energy and cellular processes in cyanobacteria are regulated by the circadian mechanism, and/or follow the rhythmicity of light-dark cycles. The temporal separation of metabolic processes is especially essential for nitrogen fixation because of inactivation of the nitrogenase by oxygen. Using a microarray approach, we analyzed gene expression in cultures of Crocosphaera watsonii WH 8501 (C. watsonii) over a 24-h period and compared the whole-genome transcription with that in Cyanothece sp. ATCC 51142 (Cyanothece), a unicellular diazotroph that inhabits coastal marine waters. Similar to Cyanothece, regulation at the transcriptional level in C. watsonii was observed for all major metabolic and energy processes including photosynthesis, carbohydrate and amino acid metabolisms, respiration, and nitrogen fixation. Increased transcript abundance for iron acquisition genes by the end of the day appeared to be a general pattern in the unicellular diazotrophs. In contrast, genes for some ABC transporters (for example, phosphorus acquisition), DNA replication, and some genes encoding hypothetical proteins were differentially expressed in C. watsonii only. Overall, C. watsonii showed a higher percentage of genes with light-dark cycling patterns than Cyanothece, which may reflect the habitats preferences of the two cyanobacteria. This study represents the first whole-genome expression profiling in cultivated Crocosphaera, and the results will be useful in determining the basal physiology and ecology of the endemic Crocosphaera populations.

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Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

et al. 2010

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“…The process elucidated by the molecular-level measurements described here appears to be of global importance. With rising atmospheric CO 2 suggested to cause increases in marine nitrogen fixation (45), as well as a potential decrease in iron availability to marine phytoplankton in general (46), understanding the biochemical adaptations for iron scarcity in diazotrophs and their implications for marine primary productivity will be of increasing importance.…”

Section: Resultsmentioning

confidence: 99%

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Saito¹,

Bertrand²,

Dutkiewicz

et al. 2011

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

202

228

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The marine nitrogen fixing microorganisms (diazotrophs) are a major source of nitrogen to open ocean ecosystems and are predicted to be limited by iron in most marine environments. Here we use global and targeted proteomic analyses on a key unicellular marine diazotroph Crocosphaera watsonii to reveal large scale diel changes in its proteome, including substantial variations in concentrations of iron metalloproteins involved in nitrogen fixation and photosynthesis, as well as nocturnal flavodoxin production. The daily synthesis and degradation of enzymes in coordination with their utilization results in a lowered cellular metalloenzyme inventory that requires ∼40% less iron than if these enzymes were maintained throughout the diel cycle. This strategy is energetically expensive, but appears to serve as an important adaptation for confronting the iron scarcity of the open oceans. A global numerical model of ocean circulation, biogeochemistry and ecosystems suggests that Crocosphaera's ability to reduce its iron-metalloenzyme inventory provides two advantages: It allows Crocosphaera to inhabit regions lower in iron and allows the same iron supply to support higher Crocosphaera biomass and nitrogen fixation than if they did not have this reduced iron requirement.cyanobacteria | marine iron cycle | nitrogen cycle

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“…We expected to possibly see differences among the groups in responses to iron, because iron requirements may vary among diazotrophs and with environmental factors. It was recently shown that elevated CO 2 concentrations may reduce Fe requirements in Crocosphaera (Fu et al, 2008). UCYN-A does not have Photosystem II (Zehr et al, 2007a), which has three Fe atoms (Raven, 1990), thus it may require less iron than the photoautotrophic diazotrophs Crocosphaera and Trichodesmium.…”

Section: Responses In Unicellular Diazotrophsmentioning

confidence: 99%

Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean

et al. 2011

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Growth limitation of phytoplankton and unicellular nitrogen (N2) fixers (diazotrophs) were investigated in the oligotrophic Western South Pacific Ocean. Based on change in abundances of nifH or 23S rRNA gene copies during nutrient-enrichment experiments, the factors limiting net growth of the unicellular diazotrophs UCYN-A (Group A), Crocosphaera watsonii, γ-Proteobacterium 24774A11, and the non-diazotrophic picocyanobacterium Prochlorococcus, varied within the region. At the westernmost stations, numbers were enhanced by organic carbon added as simple sugars, a combination of iron and an organic chelator, or iron added with phosphate. At stations nearest the equator, the nutrient-limiting growth was not apparent. Maximum net growth rates for UCYN-A, C. watsonii and γ-24774A11 were 0.19, 0.61 and 0.52 d−1, respectively, which are the first known empirical growth rates reported for the uncultivated UCYN-A and the γ-24774A11. The addition of N enhanced total phytoplankton biomass up to 5-fold, and the non-N2-fixing Synechococcus was among the groups that responded favorably to N addition. Nitrogen was the major nutrient-limiting phytoplankton biomass in the Western South Pacific Ocean, while availability of organic carbon or iron and organic chelator appear to limit abundances of unicellular diazotrophs. Lack of phytoplankton response to nutrient additions in the Pacific warm pool waters suggests diazotroph growth in this area is controlled by different factors than in the higher latitudes, which may partially explain previously observed variability in community composition in the region.

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Interactions between changing pCO2, N2 fixation, and Fe limitation in the marine unicellular cyanobacterium Crocosphaera

Cited by 145 publications

References 55 publications

Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean

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