Use of cyanobacterial gas vesicles as oxygen carriers in cell culture

Sundararajan, Anand; Ju, Lu‐Kwang

doi:10.1007/s10616-007-9044-9

Cited by 18 publications

(10 citation statements)

References 40 publications

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“…The observations made in this study now provide an opportunity to characterize gas vesicle production and regulation comprehensively in this highly genetically tractable bacterium. Finally, these discoveries (including the efficient engineering and reconstruction of gas vesicle production in E. coli) could enable facile and obvious routes to exploitation of gas vesicles for diverse biotechnological processes, including uses in gas transfer in mammalian cell culture, engineering of new antigen presentation nanotechnology systems, and for ecological control of toxic blooms (3,24,25).…”

Section: Discussionmentioning

confidence: 99%

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

Ramsay

Williamson

Spring

et al. 2011

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

128

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Gas vesicles are hollow intracellular proteinaceous organelles produced by aquatic Eubacteria and Archaea, including cyanobacteria and halobacteria. Gas vesicles increase buoyancy and allow taxis toward air-liquid interfaces, enabling subsequent niche colonization. Here we report a unique example of gas vesicle-mediated flotation in an enterobacterium; Serratia sp. strain ATCC39006. This strain is a member of the Enterobacteriaceae previously studied for its production of prodigiosin and carbapenem antibiotics. Genes required for gas vesicle synthesis mapped to a 16.6-kb gene cluster encoding three distinct homologs of the main structural protein, GvpA. Heterologous expression of this locus in Escherichia coli induced copious vesicle production and efficient cell buoyancy. Gas vesicle morphogenesis in Serratia enabled formation of a pelliclelike layer of highly vacuolated cells, which was dependent on oxygen limitation and the expression of ntrB/C and cheY-like regulatory genes within the gas-vesicle gene cluster. Gas vesicle biogenesis was strictly controlled by intercellular chemical signaling, through an N-acyl homoserine lactone, indicating that in this system the quorum-sensing molecule acts as a morphogen initiating organelle development. Flagella-based motility and gas vesicle morphogenesis were also oppositely regulated by the small RNA-binding protein, RsmA, suggesting environmental adaptation through physiological control of the choice between motility and flotation as alternative taxis modes. We propose that gas vesicle biogenesis in this strain represents a distinct mechanism of mobility, regulated by oxygen availability, nutritional status, the RsmA global regulatory system, and the quorum-sensing morphogen.vacuole | ecological adaptation | microcompartment | intercellular signaling | macromolecular assembly

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Section: Discussionmentioning

confidence: 99%

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

Ramsay

Williamson

Spring

et al. 2011

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

128

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“…As mentioned earlier, Y X/N for A. flos-aquae CCAP 1403/13f growing on nitrate as N source was determined at 17 ( 2 g cells/g N in a previous study (22). Note that common heterotrophic bacteria have approximately 12-14% of N content and, accordingly, Y X/N ∼ 7 g cells/g N (32,33).…”

Section: Resultsmentioning

confidence: 92%

“…The proportionality is governed stoichiometrically by the cell yield from N (Y X/N , g cells/g N) and the heterocyst fraction in the culture [H/(V + H)]. For the same culture growing on nitrate as the N-source, a previous study in this laboratory has determined that Y X/N ) 17 ( 2 g cells/g N (22). The fixationdependent growth is also affected by the light intensity, which effect is incorporated in the changing of r NF with I, as described in the following subsection.…”

Section: Modelmentioning

confidence: 99%

Modeling Culture Profiles of the Heterocystous N₂‐Fixing Cyanobacterium Anabaenaflos‐aquae

Pinzón

2006

Biotechnology Progress

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Heterocyst differentiation is a unique feature of nitrogen-fixing cyanobacteria, potentially important for photobiological hydrogen production. Despite the significant advances in genetic investigation on heterocyst differentiation, there were no quantitative culture-level models that describe the effects of cellular activities and cultivation conditions on the heterocyst differentiation. Such a model was developed in this study, incorporating photosynthetic growth of vegetative cells, heterocyst differentiation, self-shading effect on light penetration, and nitrogen fixation. The model parameters were determined by fitting experimental results from the growth of the heterocystous cyanobacterium Anabaena flos-aquae CCAP 1403/13f in media without and with different nitrate concentrations and under continuous illumination of white light at different light intensities (2, 5, 10, 17, 20 and 50 microE m-2 s-1). The model describes the experimental profiles well and gives reasonable predictions even for the transition of growth from that on external N source to that via nitrogen fixation, responding to the change in external N concentrations. The significance and implications of the best-fit values of the model parameters are discussed.

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“…investigators have developed oxygen carriers, such as hemoglobin, hydrocarbons, perfluorochemicals, and cyanobacterial gas vesicles. However, the instability, potential toxicity and side effects of these agents complicate their employment [19–23]. Despite this, it may be worthwhile to investigate their effects in trophoblast cell cultures.…”

Section: Discussionmentioning

confidence: 99%

Pericellular oxygen concentration of cultured primary human trophoblasts

2013

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Introduction Oxygen is pivotal in placental development and function. In vitro culture of human trophoblasts provides a useful model to study this phenomenon, but a hotly debated issue is whether or not the oxygen tension of the culture conditions mimics in vivo conditions. We tested the hypothesis that ambient oxygen tensions in culture reflect the pericellular oxygen levels. Methods We used a microelectrode oxygen sensor to measure the concentration of dissolved oxygen in the culture medium equilibrated with 21%, 8% or <0.5% oxygen. Results The concentration of oxygen in medium without cells resembled that in the ambient atmosphere. The oxygen concentration present in medium bathing trophoblasts was remarkably dependent on the depth within the medium where sampling occurred, and the oxygen concentration within the overlying atmosphere was not reflected in medium immediately adjacent to the cells. Indeed, the pericellular oxygen concentration was in a range that most would consider severe hypoxia, at ≤ 0.6% oxygen or about 4.6 mm Hg, when the overlying atmosphere was 21% oxygen. Conclusions We conclude that culture conditions of 21% oxygen are unable to replicate the pO2 of 40–60 mm Hg commonly attributed to the maternal blood in the intervillous space in the second and third trimesters of pregnancy. We further surmise that oxygen atmospheres in culture conditions between 0.5% and 21% provide different oxygen fluxes in the immediate pericellular environment yet can still yield insights into the responses of human trophoblast to different oxygen conditions.

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Use of cyanobacterial gas vesicles as oxygen carriers in cell culture

Cited by 18 publications

References 40 publications

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

Modeling Culture Profiles of the Heterocystous N₂‐Fixing Cyanobacterium Anabaenaflos‐aquae

Pericellular oxygen concentration of cultured primary human trophoblasts

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Use of cyanobacterial gas vesicles as oxygen carriers in cell culture

Cited by 18 publications

References 40 publications

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

A quorum-sensing molecule acts as a morphogen controlling gas vesicle organelle biogenesis and adaptive flotation in an enterobacterium

Modeling Culture Profiles of the Heterocystous N2‐Fixing Cyanobacterium Anabaenaflos‐aquae

Pericellular oxygen concentration of cultured primary human trophoblasts

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Modeling Culture Profiles of the Heterocystous N₂‐Fixing Cyanobacterium Anabaenaflos‐aquae