In contrast, thylakoid membranes in Cyanothece are radially arranged, extending from the cell periphery into the cell interior, demonstrating a new type of membrane organization in a cyanobacterium.
In both organisms, the thylakoid membranes are a separate system discontinuous from the plasma membrane. While the thylakoid membrane sheets in Synechocystis have been found to be disconnected from each other, in Cyanothece , thylakoid membranes form a network that extends throughout the cell.
This Cyanothece thylakoid network is stable throughout the diurnal period, even as adjacent inclusion bodies are accumulated and degraded. The multiple-branching structure by which the thylakoid membrane network is perpetuated throughout the Cyanothece cell suggests that this is a mechanism for thylakoid membrane biogenesis.
Furthermore, the thylakoid membrane network has a specific architecture: thylakoids displays a rudimentary helical organization, a potential evolutionary step to the modern grana and stroma thylakoid arrangement in plant chloroplasts. Apparently, each cyanobacterial strain has a unique ultrastructure that facilitates the accomplishment of the many specific metabolic functions required within the same single cell.
Call : LD PhD L Liberton, Michelle, "Membrane Systems in Cyanobacteria" Retrospective Theses and Dissertations. Advanced Search. Privacy Copyright. According to our reconstructions, a single evolutionary event led to the origin of parallel thylakoid arrangement, either from fascicular Figure 8 or convergent parietal Figure 9 ancestors. It is similar to the radial type with thylakoids perpendicular to cell wall, however forming an irregular network in the cell center.
The exact three-dimensional structure is unknown. This architecture emerged among other unicellular cyanobacteria in our SSU rRNA tree Figure 8 , which contradicts the previously reported position of C. Its phylogenetic position requires future confirmation, ideally using whole-genome sequencing data. Both evolutionary hypotheses agree in the ancestral position of thylakoid absence, plesiomorphic character of parietal types, and the probable direct emergence of the irregular type from the fascicular architecture.
On the other hand, single origin of the parietal arrangement, as well as speculation about evolutionary links between parallel or Cynaothece -like type and the radial type are clearly contradicted by our results. Is the thylakoid architecture a good taxonomic character in cyanobacteria? Based on our results we can conclude that thylakoid arrangements are too unstable and burdened by convergence to be used as a taxonomic character separating cyanobacterial orders, families, and, in some instances, even genera.
Unfortunately, the situation resembles those reached with other phenotypic features such as multicellularity Schirrmeister et al. The absence of thylakoids is taxonomically informative, as it is exclusive for Gloeobacter Gloeobacterales.
On the other hand, parietal arrangement, unless split and re-defined in future, does not seem to be a useful general character due to both homoplasy and plesiomorphy. The paraphyletic parietal thylakoid architecture in derived clades applies, e. Nevertheless, particular deviations of the parietal arrangement Figure 5 may help characterizing individual taxa in combination with other traits.
In Nostocales, the fascicular organization prevails in members of the rarely branching and akinete-forming family Nostocaceae Flores and Herrero, ; Ramirez et al. However, neither these taxa are entirely monophyletic Figure 8. Although very conspicuous, radial thylakoid architecture does not serve as a suitable taxonomic marker.
It seems to have serially emerged in a number of genera of the phylogenetically overlapping families Coleofasciculaceae Casamatta et al.
In spite of a possible common tendency to form radial thylakoids in certain lineages, they usually occur in individual strains, intermixed with strains exhibiting other arrangements Figure 8.
The parallel thylakoid architecture and the special type found in Cyanothece sensu stricto have each emerged only once, and therefore can serve as synapomorphies of Cyanobacteriaceae and Cyanothecaceae, respectively.
Based on this, we can also suggest including Geminocystis in the family Cyanobacteriaceae. The evolution of thylakoid organization roughly copies the phylogeny of housekeeping loci Figures 8 , 9.
This has been partly suggested by our morphometric analysis Figure 7 and convergence of radial architecture in Phormidium -like cyanobacteria Figure 8. This issue is closely related to the occurrence of special traits in cyanobacterial thylakoid architecture.
For example, characteristic spherical formations have been recorded in cyanobacteria with both parietal Taton et al. The spherical lamellae were documented to contain carboxysomes Sinetova et al. In our study, an extreme case showing cells entirely filled with spherical formations was found in Arthrospira sp.
PCC Figures 3C,D , although typically, Arthrospira strains seem to have a thylakoid arrangement similar to the radial one van Eykelenburg, ; Peduzzi et al. However, some lineages tend to contain spherical formations more than others Figure 8. Similarly, a dense subperipheral layer of thylakoids was observed in S. Finally, superficial analysis can distinguish special types that are consequence of the fact that standard TEM provides only a snapshot crossing a single cell in a single plane.
An example of this probably is the triangular parietal arrangement documented in several taxa Nierzwicki-Bauer et al. In our opinion, it demonstrates a frequent presence of three peripheral fascicles of thylakoids in these clades. However, the same strains can also contain just two fascicles when viewed in a different TEM section Nierzwicki-Bauer et al. We have not found any single protein whose phylogeny would be precisely in accordance with individual thylakoid types.
This is however not extremely surprising. Functional variability of homologous proteins tends to be governed rather by their tertiary structure maintained by complementary changes, and by the replacement of individual ligand-binding residues rather than primary amino acid sequence used in standard phylogenetic analysis Pils et al. Regulation of cellular processes at expression level and protein interactions may also be responsible for the observed variability in phenotypes.
From this point of view, transcriptomic and proteomic analyses, and ultimately comparisons among structural models of the particular proteins are essential next steps in future research. Another explanation, supported by our morphometric analysis Figure 7 , implies that cellular mechanisms, including various regulatory elements responsible for cell size and morphology affect also the morphology of thylakoids. Similarly, proteins regulating cell division of filamentous cyanobacteria could possibly influence the morphology of radial type of thylakoids.
These possibilities are largely unexplored, and their investigation was beyond the scope of the current study. Interestingly, homologs of several proteins postulated to be involved in thylakoid or chloroplast biogenesis and morphology were found only in limited number of cyanobacteria or were completely missing. For example, the thylakoid curvature protein CurT Armbruster et al.
As previously demonstrated, deletion in curT resulted in disrupted thylakoid organization and absence of biogenesis centers in Synechocystis Heinz et al. Our results contradict the universal function of CurT in membrane architecture and suggest that CurT is not an universally essential factor for proper thylakoid biogenesis in cyanobacteria.
Similarly, a TerC homolog can be found only in a very limited number of cyanobacteria, but remarkably including the thylakoid-less Gloeobacter. In Arabidopsis , TerC mutants are unable to accumulate newly synthesized thylakoid membrane proteins, which led to an assumption that TerC acts in insertion of thylakoid membrane proteins Kwon and Cho, ; Theis and Schroda, In summary, it seems that the molecular mechanisms involved in thylakoid biogenesis and spatial organization substantially vary among cyanobacteria.
Experimental discoveries made in plant chloroplasts or selected experimental strains of cyanobacteria can therefore rarely be generalized. Raw datasets generated for statistical analysis and ancestral state reconstruction are included in the Supplementary Files.
Raw sequence alignment data supporting the conclusions of this manuscript will be made available by the authors, without undue reservation, to any qualified researcher.
JM and OS collected the data and performed the phylogenetic and bioinformatic analyses. JM performed the statistical analyses. LB and JM prepared the line drawings. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Liberton, M. II, Berg, R. Insights into the complex 3-D architecture of thylakoid membranes in unicellular cyanobacterium Cyanothece sp. The middle lamella forms the outermost layer and is depicted as a flat, translucent, blue slab. Many pectin molecules are shown inside the middle lamella. In this layer, the pectin molecules are represented as light-green strands with some curvature. The middle lamella also contains soluble proteins similar to those in the primary cell wall.
Lignin is not shown. The cell wall surrounds the plasma membrane of plant cells and provides tensile strength and protection against mechanical and osmotic stress. It also allows cells to develop turgor pressure , which is the pressure of the cell contents against the cell wall. Plant cells have high concentrations of molecules dissolved in their cytoplasm, which causes water to come into the cell under normal conditions and makes the cell's central vacuole swell and press against the cell wall.
With a healthy supply of water, turgor pressure keeps a plant from wilting. In drought, a plant may wilt, but its cell walls help maintain the structural integrity of its stems, leaves, and other structures, despite a shrinking, less turgid vacuole.
Plant cell walls are primarily made of cellulose , which is the most abundant macromolecule on Earth. Cellulose fibers are long, linear polymers of hundreds of glucose molecules. These fibers aggregate into bundles of about 40, which are called microfibrils.
Microfibrils are embedded in a hydrated network of other polysaccharides. The cell wall is assembled in place. Precursor components are synthesized inside the cell and then assembled by enzymes associated with the cell membrane Figure 3. Plant cells additionally possess large, fluid-filled vesicles called vacuoles within their cytoplasm. Vacuoles typically compose about 30 percent of a cell's volume, but they can fill as much as 90 percent of the intracellular space.
Plant cells use vacuoles to adjust their size and turgor pressure. Vacuoles usually account for changes in cell size when the cytoplasmic volume stays constant.
Some vacuoles have specialized functions, and plant cells can have more than one type of vacuole. Vacuoles are related to lysosomes and share some functions with these structures; for instance, both contain degradative enzymes for breaking down macromolecules. Vacuoles can also serve as storage compartments for nutrients and metabolites. For instance, proteins are stored in the vacuoles of seeds, and rubber and opium are metabolites that are stored in plant vacuoles.
This page appears in the following eBook. Aa Aa Aa. Plant Cells, Chloroplasts, and Cell Walls. Plant cells have several structures not found in other eukaryotes. In particular, organelles called chloroplasts allow plants to capture the energy of the Sun in energy-rich molecules; cell walls allow plants to have rigid structures as varied as wood trunks and supple leaves; and vacuoles allow plant cells to change size. What Is the Origin of Chloroplasts?
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