Cyanobacterial ultrastructure in light of genomic sequence data

Gonzalez-Esquer, C. Raul; Šmarda, Jan; Rippka, Rosmarie; Axen, Seth D.; Guglielmi, Gérard; Gugger, Muriel; Kerfeld, Cheryl A.

doi:10.1007/s11120-016-0286-2

Cited by 37 publications

(26 citation statements)

References 45 publications

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“…Cell walls of Gloeocapsa sp. PCC 7428 have been shown to be composed of a thick extracellular sheath of mucopolysaccharides (Gonzalez‐Esquer et al., ), which may therefore be responsible for this relatively high Ca sorption capability. Whether this is due to a high surface Ca adsorption capacity of the strain and/or precipitation of extracellular Ca‐mineral phases could not be determined here but it is known that there is a continuum between surface adsorption and extracellular mineral precipitation (Warren & Ferris, ).…”

Section: Discussionmentioning

confidence: 99%

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

et al. 2019

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Several species of cyanobacteria biomineralizing intracellular amorphous calcium carbonates (ACC) were recently discovered. However, the mechanisms involved in this biomineralization process and the determinants discriminating species forming intracellular ACC from those not forming intracellular ACC remain unknown. Recently, it was hypothesized that the intensity of Ca uptake (i.e., how much Ca was scavenged from the extracellular solution) might be a major parameter controlling the capability of a cyanobacterium to form intracellular ACC. Here, we tested this hypothesis by systematically measuring the Ca uptake by a set of 52 cyanobacterial strains cultured in the same growth medium. The results evidenced a dichotomy among cyanobacteria regarding Ca sequestration capabilities, with all strains forming intracellular ACC incorporating significantly more calcium than strains not forming ACC. Moreover, Ca provided at a concentration of 50 μM in BG‐11 was shown to be limiting for the growth of some of the strains forming intracellular ACC, suggesting an overlooked quantitative role of Ca for these strains. All cyanobacteria forming intracellular ACC contained at least one gene coding for a mechanosensitive channel, which might be involved in Ca influx, as well as at least one gene coding for a Ca2+/H+ exchanger and membrane proteins of the UPF0016 family, which might be involved in active Ca transport either from the cytosol to the extracellular solution or the cytosol toward an intracellular compartment. Overall, massive Ca sequestration may have an indirect role by allowing the formation of intracellular ACC. The latter may be beneficial to the growth of the cells as a storage of inorganic C and/or a buffer of intracellular pH. Moreover, high Ca scavenging by cyanobacteria biomineralizing intracellular ACC, a trait shared with endolithic cyanobacteria, suggests that these cyanobacteria should be considered as potentially significant geochemical reservoirs of Ca.

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Section: Discussionmentioning

confidence: 99%

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

et al. 2019

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“…Therefore, it will be interesting to compare the ATPase activities of the two McdA types, as well as the stimulatory activities of their respective McdB proteins. How Type 1 and Type 2 systems differ mechanistically, and whether these differences correlate to known factors influencing carboxysome positioning such as carboxysome size and quantity (Gonzalez-Esquer et al, 2016; MacCready et al, 2018) , genome copy number and volume (Griese et al, 2011) , redox state of cells (Sun et al, 2016, 2019) , and McdAB stoichiometry (MacCready et al, 2018) , as well as unknown factors including McdB LLPS behavior and/or intracellular salt/pH conditions (see below), is important for understanding the diversity and evolution of the McdAB system among cyanobacteria.…”

Section: Discussionmentioning

confidence: 99%

The McdAB Carboxysome Positioning System is Widespread Among β-cyanobacteria

MacCready

Basalla

Vecchiarelli

2019

Preprint

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SummaryCarboxysomes are protein-based organelles that are essential for allowing cyanobacteria to fix CO2. Previously we identified a two-component system, McdAB, responsible for equidistantly positioning carboxysomes in the model cyanobacterium Synechococcus elongatus PCC 7942. McdA, a ParA-type ATPase, non-specifically binds the nucleoid in the presence of ATP. McdB, a novel factor that directly binds carboxysomes, displaces McdA from the nucleoid. Removal of McdA from the nucleoid in the vicinity of carboxysomes by McdB causes a global break in McdA symmetry, and carboxysome motion occurs via a Brownian-ratchet based mechanism towards the highest concentration of McdA. Despite the importance for cyanobacteria to properly position their carboxysomes, whether the McdAB system is widespread among cyanobacteria remains an open question. Here, we used neighborhood analysis to show that the McdAB system is widespread among β-cyanobacteria and often clusters near carboxysome-related components. Moreover, we show that two distinct McdAB systems exist in β-cyanobacteria, with Type 2 systems being the most abundant (>98% of β-cyanobacteria) and Type 1 systems, like that of S. elongatus, possibly being acquired more recently. Surprisingly, our analysis suggests that the McdAB system is completely absent in α-cyanobacteria. Lastly, all McdB proteins we identified share the sequence signatures of a protein capable of undergoing Liquid-Liquid Phase Separation (LLPS). Indeed, we find that S. elongatus McdB undergoes LLPS in vitro, the first example of a ParA-type ATPase partner protein exhibiting this behavior. This is an intriguing finding given the recent demonstration of LLPS activity by β-carboxysome core components. Our results have broader implications for understanding carboxysome biogenesis and positioning across all β-cyanobacteria.In BriefWe found that the McdAB carboxysome positioning system is widespread among β-cyanobacteria, absent in α-cyanobacteria, exists in two distinct forms, and that S. elongatus McdB undergoes liquid-liquid phase separation.

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“…Initially, TDX16 cells (day 1) were surrounded by thick sheaths and enclosed within the sporangia ( Figure 6 and Figure 7), resembling the endospores (baeocytes) of cyanobacterium Chroococcidiopsis sp. [19] and Chroococcidiopsis thermalis [20]. TDX16 cells in the same or different sporangia remained at different states with some different inclusions ( Figure 6 cyanobacterial inclusions, including carboxysomes (CX) [21], polyphosphate bodies (PB) [22] and osmiophilic granules (OG) [23].…”

Section: Initial Structure Of Tdx16 Cellsmentioning

confidence: 99%

De Novo Organelle Biogenesis in the Cyanobacterium TDX16 Released from the Green Alga <i>Haematococcus pluvialis</i>

Dong¹,

Xing²,

Han³

et al. 2020

CellBio

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It is believed that eukaryotes arise from prokaryotes, which means that organelles can form de novo in prokaryotes. Such events, however, had not been observed previously. Here, we report the biogenesis of organelles in the endosymbiotic cyanobacterium TDX16 (prokaryote) that was released from its senescent/necrotic host cell of green alga Haematococcus pluvialis (eukaryote).Microscopic observations showed that organelle biogenesis in TDX16 initiated with cytoplasm compartmentalization, followed by de-compartmentalization, DNA allocation, and re-compartmentalization, as such two composite organelles-the primitive chloroplast and primitive nucleus sequestering minor and major fractions of cellular DNA respectively were formed. Thereafter, the eukaryotic cytoplasmic matrix was built up from the matrix extruded from the primitive nucleus; mitochondria were assembled in and segregated from the primitive chloroplast, whereby the primitive nucleus and primitive chloroplast matured into the nucleus and chloroplast respectively. While mitochondria subsequently turned into double-membraned vacuoles after matrix degradation. Results of pigment analyses, 16S rRNA and genome sequencing revealed that TDX16 is a phycocyanin-containing cyanobacterium resembling Chroococcidiopsis thermalis, which had acquired 9,017,401 bp DNAs with 10,301 genes from its host. Accordingly, we conclude that organelle biogenesis in TDX16 is achieved by hybridizing the acquired eukaryotic DNAs with its own one and expressing the hybrid genome. The formation of organelles in cyanobacterium TDX16 is the first case of organelle biogenesis in prokaryotes observed so far, which sheds an unprecedented light on eukaryotes and their connections with prokaryotes, and thus has broad implications on biology.The transition of cyanobacterium TDX16 cells into green algal cells is the first case of prokaryote-to-eukaryote transition observed so far, which provides the opportunity and platform to solve the puzzle of organelle biogenesis in prokaryotic cells. Hence, this study aims to investigate how and why organelles form in cyanobacterium TDX16. Materials and Methods Strain and CultivationPure TDX16 cells were collected from the H. pluvialis cultures, in which all H. pluvialis cells burst and released TDX16 cells [11], and maintained in sterile BG-11 liquid medium [13] at 25˚C, 12 μmol photons m −2 •s −1 in the illumination incubator. Axenic TDX16 was prepared according to the method [14] with some modifications. Briefly, pure TDX16 culture was treated with antibiotics nystatin (100 μg/ml) and cycloheximide (150 μg/ml) for 18 h, then the culture was diluted 10 fold with sterile distilled water and plated onto BG-11 solid medium in petri dishes supplemented (w/v)with glucose (0.5%), peptone (0.3%) and yeast extracts (0.2%). The petri dishes were sealed with parafilm and incubated in an inverted position in the illumination incubator at 25˚C, 12 μmol photons m −2 •s −1 for one month. The colonies (Figure 4) were picked and transferred into autoclaved 250-ml flasks ...

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Cyanobacterial ultrastructure in light of genomic sequence data

Cited by 37 publications

References 45 publications

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

The McdAB Carboxysome Positioning System is Widespread Among β-cyanobacteria

De Novo Organelle Biogenesis in the Cyanobacterium TDX16 Released from the Green Alga <i>Haematococcus pluvialis</i>

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Cyanobacterial ultrastructure in light of genomic sequence data

Cited by 37 publications

References 45 publications

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO3 and impact on their growth

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO3 and impact on their growth

The McdAB Carboxysome Positioning System is Widespread Among β-cyanobacteria

De Novo Organelle Biogenesis in the Cyanobacterium TDX16 Released from the Green Alga &lt;i&gt;Haematococcus pluvialis&lt;/i&gt;

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Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

De Novo Organelle Biogenesis in the Cyanobacterium TDX16 Released from the Green Alga <i>Haematococcus pluvialis</i>