Changes in thylakoid structure associated with the differentiation of heterocysts in the cyanobacterium, Anabaena cylindrica

Giddings, Thomas H.; Staehelin, L. Andrew

doi:10.1016/0005-2728(79)90074-4

Cited by 41 publications

(13 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…10). The histogram of particle sizes on the E-face of the cyanelles' thylakoids closely resembles corresponding histograms derived from cyanobacteria (12), red algal chloroplasts (31), and Cyanidium (39), all of which show a large population of particles measuring about 10 nm in diameter. Together with the previous studies (12,31,39) that suggest that the 10-nm E-face particles represent PSII centers, our findings support the hypothesis that phycobilisomes on the thylakoid surface are in direct contact with PSII centers within the membrane.…”

Section: Discussionsupporting

confidence: 64%

“…Inasmuch as the majority of light energy absorbed by phycobiliproteins is transferred initially to PSII (17,33,37), it has been proposed (but not directly demonstrated) that the aligned E-face particles are PSII complexes and are in direct contact with rows of phycobilisomes (31). Independent lines of evidence suggesting that these 10-nm E-face particles are PSII centers are that: (a) they are absent from the thylakoids of cyanobacterial heterocysts (12) which lack PSII; and (b) they are more numerous in PSII-enriched mutants of Cyanidium (39). Our findings support the hypothesis that such PSII complexes are directly associated with phycobilisomes on the thylakoid surface.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Structure of the Thylakoids and Envelope Membranes of the Cyanelles of Cyanophora paradoxa

Giddings¹,

Wasmann²,

Staehelin³

1983

Plant Physiol.

Self Cite

121

View full text Add to dashboard Cite

The cyanelles of Cyanophora paradoxa Korsch. are photosynthetically active obligate endosymbionts in which phycobiliproteins serve as the major accessory pigments. Freeze-fracture electron micrographs of thylakoids in isolated cyanelies reveal long parallel rows of particles covering most of the E-face, while a more random particle arrangement is evident in some areas. The center-to-center spacing of particles within these rows is about 10 nanometers. Their mean diameter was measured at 9.4 nanometers. The particles on the P-face have a mean diameter of 7.2 nanometers. Thylakoids that retained nearly the full complement of phycobiliproteins (determined spectrophotometrically and by gel electrophoresis) were isolated from the cyanelies. In thin sections of these preparations, rows of disc-shaped phycobilisomes are evident on the surface of the thylakoids. The spacing of the rows of phycobilisomes corresponds to that of the rows of E-face particles (approximately 45 nanometers, center to center). The periodicity of the disc-shaped phycobilisomes within a row is 10 nanometers suggesting a one-to-one association between phycobilisomes and E-face particles.In addition, visualization of the protoplasmic surface (PS) of isolated thylakoids by freeze-etch electron microscopy shows that rows of discshaped phycobilisomes are aligned directly above rows of particles exhibiting two subunits, presumably the P-surface projections of the 10-nanometer intramembrane particles. These observations, together with earlier studies indicating that the 10-nanometer E-face particles probably represent photosystem II (PSII) complexes, suggest that phycobilisomes are positioned on the thylakoid surface in direct contact with PSII centers within the thylakoid membrane.The inner envelope membrane of the cyanelles, observed in freezefracture replicas, resembles cyanobacterial plasma membranes and is dissimilar to the chloroplast envelope membranes of red or green algae.The envelope of isolated cyanelies exhibits two additional layers: (a) a 5-to 7-nanometer-thick layer that lies adjacent to the inner membrane and which seems to correspond to the peptidoglycan layer of cyanobacteria; and (b) a layer external to the purported peptidoglycan layer that exhibits fracture faces similar to those of the lipopolysaccharide layer of gram negative bacteria. Our findings indicate that the supramolecular architecture of cyanelles differs only slightly from free-living cyanobacteria to which they are presumably related.Cyanobacteria, red algal chloroplasts and certain cyanobacteria- like endosymbionts, termed cyanelles, employ phycobiliproteins attached to the outer surface of their thylakoids as the major lightharvesting pigments for 02-evolving photosynthesis (3,7,10,29,35). In the atypical case of Gloeobacter violaceus, the phycobilisomes are attached to the plasma membrane (15). The cyanelles of Cyanophora paradoxa are generally regarded as cyanobacterial endosymbionts within a flagellated unicellular eukaryote (16,30,34). According to the end...

show abstract

Section: Discussionsupporting

confidence: 64%

mentioning

confidence: 99%

Structure of the Thylakoids and Envelope Membranes of the Cyanelles of Cyanophora paradoxa

Giddings¹,

Wasmann²,

Staehelin³

1983

Plant Physiol.

Self Cite

121

View full text Add to dashboard Cite

show abstract

“…The model of the PS II dimer is primarily based on freeze-fracture electron microscopic studies and crystallographic models. The freeze-fracture studies revealed the presence of pairs of 10 nm particles associated with phycobilisomes, which were suggested to be the dimeric forms of PS II (55)(56)(57). PS II monomers could associate together to form a dimer in some physiological statuses.…”

Section: Discussionmentioning

confidence: 99%

Photosystem II Complex in Vivo Is a Monomer

Takahashi

Inoue-Kashino

Ozawa

et al. 2009

Journal of Biological Chemistry

View full text Add to dashboard Cite

Photosystem II (PS II) complexes are membrane protein complexes that are composed of >20 distinct subunit proteins. Similar to many other membrane protein complexes, two PS II complexes are believed to form a homo-dimer whose molecular mass is ϳ650 kDa. Contrary to this well known concept, we propose that the functional form of PS II in vivo is a monomer, based on the following observations. Deprivation of lipids caused the conversion of PS II from a monomeric form to a dimeric form. Only a monomeric PS II was detected in solubilized cyanobacterial and red algal thylakoids using blue-native polyacrylamide gel electrophoresis. Furthermore, energy transfer between PS II units, which was observed in the purified dimeric PS II, was not detected in vivo. Our proposal will lead to a re-evaluation of many crystallographic models of membrane protein complexes in terms of their oligomerization status. Photosystem II (PS II)3 complexes convert solar energy to biological redox energy. Through this reaction process, water molecules are oxidized and molecular oxygen is released as a byproduct (reviewed in Ref. 1), which is the only source of molecular oxygen upon which all aerobic organisms on earth rely. PS II core complexes are membrane protein complexes that are composed of Ͼ20 distinct subunit proteins and many functional cofactors, including chlorophylls (Chls), carotenoids, plastoquinone, and metal ions (2-5). Similar to many other membrane protein complexes (6 -10), two PS II core complexes are believed to associate together to form a homodimer with a molecular mass of ϳ650 kDa, as shown by crystallographic models (2, 3, 5).The PS II complex turns over dynamically, although it is quite an integrated complex; our current understanding is that the PS II complex that is damaged by high light is disintegrated into a monomeric form and is further dissociated to replace a degraded D1 protein with a de novo synthesized D1 (reviewed in Refs. 11 and 12). After the replacement, the PS II complex is integrated into a functional form as a dimer. It is supposed that PS II subunit proteins such as PsbI (13) or PsbTc (14) participate in the formation of the PS II dimer.Crystallographic models of PS II have enabled the determination of the accurate molecular architecture of PS II complexes, all of which are in a dimeric form. The most recent crystallographic model of the PS II dimer at 3.0-Å resolution revealed the presence of six detergent molecules located at the interface of the two monomers (5). Small structural fluctuations during the purification process might allow the invasion of those detergent molecules. However, it is also probable that the PS II complexes exist in the form of a monomer in vivo and the two distinct monomers become a dimer during the purification step incorporating detergents between their interfaces. This idea led us to investigate the actual form of PS II in vivo. Contrary to the above well known dimeric model of a functional PS II core complex, here we show that the PS II core complex functions and exist...

show abstract

“…First, a homogeneous layer of polysaccharides (heterocyst envelope polysaccharides [HEPs]) is formed by deposition of the material outside the gram-negative cell wall (10,26). Subsequently, specific glycolipids (heterocyst envelope glycolipids [HGLs]) are made and deposited between this protective layer and the outer membrane, forming the socalled laminated layer (26,31). This layer is a barrier for entry of gases (31,59,61).…”

mentioning

confidence: 99%

A TolC-Like Protein Is Required for Heterocyst Development inAnabaenasp. Strain PCC 7120

Moslavac¹,

Nicolaisen²,

Mirus³

et al. 2007

J Bacteriol

View full text Add to dashboard Cite

The filamentous cyanobacterium Anabaena sp. strain PCC 7120 forms heterocysts in a semiregular pattern when it is grown on N 2 as the sole nitrogen source. The transition from vegetative cells to heterocysts requires marked metabolic and morphological changes. We show that a trimeric pore-forming outer membrane ␤-barrel protein belonging to the TolC family, Alr2887, is up-regulated in developing heterocysts and is essential for diazotrophic growth. Mutants defective in Alr2887 did not form the specific glycolipid layer of the heterocyst cell wall, which is necessary to protect nitrogenase from external oxygen. Comparison of the glycolipid contents of wild-type and mutant cells indicated that the protein is not involved in the synthesis of glycolipids but might instead serve as an exporter for the glycolipid moieties or enzymes involved in glycolipid attachment. We propose that Alr2887, together with an ABC transporter like DevBCA, is part of a protein export system essential for assembly of the heterocyst glycolipid layer. We designate the alr2887 gene hgdD (heterocyst glycolipid deposition protein).Gram-negative bacteria use a type I export system to transfer proteins or other molecules, like siderophores or fatty acids, to the cell surface (37, 50, 55). The proteinaceous substrates contain a C-terminal secretion signal essential and sufficient for export. The information for targeting and translocation, however, seems to be presented in the form of a secondary structure element rather than in the primary sequence as no clear amino acid motif has been identified. The machinery of type I export systems bridges the periplasm, allowing transfer of their substrates beyond the outer membrane. The export system is composed of a translocase spanning the plasma membrane with an ␣-helical, pore-forming domain and a cytosolic domain energizing the translocation process. Additionally, an adaptor protein associates with the translocase and, after substrate association, induces an interaction with an outer membrane TolC-like exit tunnel to conduct the secretion. Whereas TolC-like proteins from gram-negative proteobacteria have been amply investigated (37,50,54,55), nothing is known about these systems in cyanobacteria. Based on sequence similarity (40) and proteomic analysis of the cell wall fraction (42), we have recently proposed the existence of a protein of this type, Alr2887, in Anabaena sp. strain PCC 7120, for which a function in lipid transfer has previously been proposed (40).Anabaena sp. strain PCC 7120 is a filamentous cyanobacterium which starts a program of cell differentiation upon nitrogen starvation that results in the appearance of nitrogen-fixing cells. These cells are called heterocysts and are arranged in a semiregular pattern along the filament (63). Three mechanisms protect the oxygen-labile nitrogenase from irreversible inactivation by O 2 produced by oxygenic photosynthesis: (i) formation of extra envelope layers outside the gram-negative cell wall, (ii) degradation of photosystem II antennae and a d...

show abstract

Changes in thylakoid structure associated with the differentiation of heterocysts in the cyanobacterium, Anabaena cylindrica

Cited by 41 publications

References 42 publications

Structure of the Thylakoids and Envelope Membranes of the Cyanelles of Cyanophora paradoxa

Structure of the Thylakoids and Envelope Membranes of the Cyanelles of Cyanophora paradoxa

Photosystem II Complex in Vivo Is a Monomer

A TolC-Like Protein Is Required for Heterocyst Development inAnabaenasp. Strain PCC 7120

Contact Info

Product

Resources

About