Oscillin, an extracellular, Ca<sup>2+</sup>‐binding glycoprotein essential for the gliding motility of cyanobacteria

Hoiczyk, Egbert; Baumeister, Wolfgang

doi:10.1046/j.1365-2958.1997.5971972.x

Cited by 68 publications

(74 citation statements)

References 22 publications

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“…Like most S-layer proteins, AfpA contains no cysteine residues (26). S-layer and RTX proteins such as oscillin (36), SwmA, a cell surface protein required for motility in water (7), and AfpA all contain a combination of predicted calcium-binding motifs and N-glycosylation motifs (Fig. 3 and 4).…”

Section: Discussionmentioning

confidence: 99%

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

Muryoi

Sato²,

Kaneko³

et al. 2004

J Bacteriol

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The Arctic plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 secretes an antifreeze protein (AFP) that promotes survival at subzero temperatures. The AFP is unusual in that it also exhibits a low level of ice nucleation activity. A DNA fragment with an open reading frame encoding 473 amino acids was cloned by PCR and inverse PCR using primers designed from partial amino acid sequences of the isolated AFP. The predicted gene product, AfpA, had a molecular mass of 47.3 kDa, a pI of 3.51, and no previously known function. Although AfpA is a secreted protein, it lacked an N-terminal signal peptide and was shown by sequence analysis to have two possible secretion systems: a hemolysin-like, calcium-binding secretion domain and a type V autotransporter domain found in gram-negative bacteria. Expression of afpA in Escherichia coli yielded an intracellular 72-kDa protein modified with both sugars and lipids that exhibited lower levels of antifreeze and ice nucleation activities than the native protein. The 164-kDa AFP previously purified from P. putida GR12-2 was a lipoglycoprotein, and the carbohydrate was required for ice nucleation activity. Therefore, the recombinant protein may not have been properly posttranslationally modified. The AfpA sequence was most similar to cell wall-associated proteins and less similar to ice nucleation proteins (INPs). Hydropathy plots revealed that the amino acid sequence of AfpA was more hydrophobic than those of the INPs in the domain that forms the ice template, thus suggesting that AFPs and INPs interact differently with ice. To our knowledge, this is the first gene encoding a protein with both antifreeze and ice nucleation activities to be isolated and characterized.

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Section: Discussionmentioning

confidence: 99%

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

Muryoi

Sato²,

Kaneko³

et al. 2004

J Bacteriol

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“…The motile cyanobacterium Phormidium unicatum was shown previously to contain fibrillar arrays of a glycoprotein, oscillin, on top of its S-layer. The protein is conserved in motile filamentous cyanobacteria and seems to play a role in gliding motility (13). The S-layer glycoprotein SwmA was shown previously to be required in Synechococcus sp.…”

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confidence: 99%

An Extracellular Glycoprotein Is Implicated in Cell-Cell Contacts in the Toxic CyanobacteriumMicrocystis aeruginosaPCC 7806

et al. 2008

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Microcystins are the most common cyanobacterial toxins found in freshwater lakes and reservoirs throughout the world. They are frequently produced by the unicellular, colonial cyanobacterium Microcystis aeruginosa; however, the role of the peptide for the producing organism is poorly understood. Differences in the cellular aggregation of M. aeruginosa PCC 7806 and a microcystin-deficient ⌬mcyB mutant guided the discovery of a surface-exposed protein that shows increased abundance in PCC 7806 mutants deficient in microcystin production compared to the abundance of this protein in the wild type. Microcystis aeruginosa is a unicellular colonial cyanobacterium frequently producing mass developments and surface scums in freshwater habitats. Microcystis cyanobacteria are widely known for their production of the potent hepatotoxin microcystin. Microcystins are a family of cyclic heptapeptides that potently inhibit protein phosphatases of the eukaryotic protein phosphatase P family. Several cases of human and animal poisonings have been attributed to the presence of these toxins in water supplies and recreational lakes (6, 15). Microcystins are synthesized by a large enzyme complex comprising nonribosomal peptide synthetases, polyketide synthases, and tailoring enzymes (32).In the environment, Microcystis occurs as a mixture of morphotypes that differ in their cell and sheath characteristics (17). The formation of large colonies embedded in mucilage and the presence of gas vesicles enable Microcystis colonies to regulate their buoyancy (35). The ability to migrate vertically in lakes provides a significant advantage over many other phytoplankton species (1). Several studies have shown a correlation of Microcystis morphotypes with the presence of specific peptides. Microcystins are most frequently associated with M. aeruginosa and M. viridis, whereas other Microcystis morphotypes, such as M. wesenbergii and M. ichthyoblabe, usually lack these peptides (8, 34). A possible correlation of colony form and the nonribosomal peptide microcystin was further supported by the finding that microcystin influences the expression and oligomerization of a surface-exposed lectin that may facilitate the recognition and attachment of Microcystis cells (16). In addition, there is increasing evidence that microcystin released from dead cells may serve as an infochemical in the Microcystis community, thereby enhancing the fitness of surviving cells (26). The microcystin-dependent expression of the two microcystin-related proteins MrpA and MrpB that show similarity to the quorum sensing-controlled RhiA and RhiB proteins in Rhizobium leguminosarum (11) further supports the idea that microcystin may be perceived as an intercellular signal (4).In the present study, the correlation of microcystin with a novel surface-exposed component, a glycoprotein, is reported. In the past few decades, an increasing number of bacterial proteins have been shown to be glycosylated, including a wide range of different cell envelope components such as membrane-ass...

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“…However, they did observe a tetragonal S-layer external to the outer membrane and, above this, an array of helically arranged surface fibrils, 10 to 12 nm in diameter, with a regular spacing of 14 nm. The fibrils were later shown to consist of a single calcium-binding protein that was given the name oscillin (13). Hoiczyk and Baumeister concluded that the oscillin fibrils served as a screw thread guiding the rotation of the trichome, which was powered by the extrusion of slime from junctional pores that form a ring around the filament on either side of each cell septum (13,14).…”

mentioning

confidence: 99%

“…Hoiczyk and Baumeister concluded that the oscillin fibrils served as a screw thread guiding the rotation of the trichome, which was powered by the extrusion of slime from junctional pores that form a ring around the filament on either side of each cell septum (13,14). They were also able to show that spontaneous, nonmotile mutants of Phormidium uncinatum failed to produce extracellular slime and lacked the S-layer and oscillin fibrils, implying that one, or more, of these components was essential for motility.In a previous study of several motile filamentous cyanobacteria, we demonstrated the presence of a parallel array of 25-to 30-nm diameter fibrils, situated between the peptidoglycan and the OM (3); these fibrils are much wider than those reported by Halfen and Castenholz (11) and Hoiczyck and Baumeister (12,13). The OM was seen to penetrate between the rows of fibrils, and as a consequence the outer surface of the cells appeared corrugated rather than smooth.…”

mentioning

confidence: 99%

“…The fibrils were later shown to consist of a single calcium-binding protein that was given the name oscillin (13). Hoiczyk and Baumeister concluded that the oscillin fibrils served as a screw thread guiding the rotation of the trichome, which was powered by the extrusion of slime from junctional pores that form a ring around the filament on either side of each cell septum (13,14). They were also able to show that spontaneous, nonmotile mutants of Phormidium uncinatum failed to produce extracellular slime and lacked the S-layer and oscillin fibrils, implying that one, or more, of these components was essential for motility.…”

mentioning

confidence: 99%

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Nanoscale Visualization of a Fibrillar Array in the Cell Wall of Filamentous Cyanobacteria and Its Implications for Gliding Motility

Read¹,

Connell

Adams³

2007

J Bacteriol

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Many filamentous cyanobacteria are motile by gliding, which requires attachment to a surface. There are two main theories to explain the mechanism of gliding. According to the first, the filament is pushed forward by small waves that pass along the cell surface. In the second, gliding is powered by the extrusion of slime through pores surrounding each cell septum. We have previously shown that the cell walls of several motile cyanobacteria possess an array of parallel fibrils between the peptidoglycan and the outer membrane and have speculated that the function of this array may be to generate surface waves to power gliding. Here, we report on a study of the cell surface topography of two morphologically different filamentous cyanobacteria, using field emission gun scanning electron microscopy (FEGSEM) and atomic force microscopy (AFM). FEGSEM and AFM images of Oscillatoria sp. strain A2 confirmed the presence of an array of fibrils, visible as parallel corrugations on the cell surface. These corrugations were also visualized by AFM scanning of fully hydrated filaments under liquid; this has not been achieved before for filamentous bacteria. FEGSEM images of Nostoc punctiforme revealed a highly convoluted, not parallel, fibrillar array. We conclude that an array of parallel fibrils, beneath the outer membrane of Oscillatoria, may function in the generation of thrust in gliding motility. The array of convoluted fibrils in N. punctiforme may have an alternative function, perhaps connected with the increase in outer membrane surface area resulting from the presence of the fibrils.Cyanobacteria are phototrophic prokaryotes that vary in morphology from unicellular strains to filamentous forms capable of complex cellular differentiation (1, 2). Many cyanobacteria are motile. Some unicellular Synechococcus strains are capable of swimming by a mechanism that does not employ flagella (28) in which thrust is generated by an extracellular protein, SwmA (6, 19), but most motile cyanobacteria employ gliding, which requires attachment to a surface. The unicellular Synechocystis sp. strain PCC 6803 moves by a form of gliding often referred to as twitching motility, which is powered by type IV pili on the cell surface (4,5,30). In filamentous strains, in which forward movement is often accompanied by rotation of the filament about its long axis (10), the mechanism of gliding is unknown. Halfen and Castenholz proposed a model for gliding (11) based on the results of their own electron microscopy (EM) studies of motile filamentous cyanobacteria and on the theories of Jarosch (16). They speculated that the motor for gliding in the filamentous Oscillatoriaceae might be provided by proteinaceous contractile fibrils, 6 to 9 nm in diameter, located between the peptidoglycan layer and the outer membrane (OM) and that rotation of the filaments during gliding might be a result of the helical arrangement of the fibrils. An ultrastructural examination of the cell walls of four gliding filamentous cyanobacteria by Hoiczyk and Baumeister (12...

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Oscillin, an extracellular, Ca²⁺‐binding glycoprotein essential for the gliding motility of cyanobacteria

Cited by 68 publications

References 22 publications

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

An Extracellular Glycoprotein Is Implicated in Cell-Cell Contacts in the Toxic CyanobacteriumMicrocystis aeruginosaPCC 7806

Nanoscale Visualization of a Fibrillar Array in the Cell Wall of Filamentous Cyanobacteria and Its Implications for Gliding Motility

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Oscillin, an extracellular, Ca2+‐binding glycoprotein essential for the gliding motility of cyanobacteria

Cited by 68 publications

References 22 publications

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

Cloning and Expression of afpA , a Gene Encoding an Antifreeze Protein from the Arctic Plant Growth-Promoting Rhizobacterium Pseudomonas putida GR12-2

An Extracellular Glycoprotein Is Implicated in Cell-Cell Contacts in the Toxic CyanobacteriumMicrocystis aeruginosaPCC 7806

Nanoscale Visualization of a Fibrillar Array in the Cell Wall of Filamentous Cyanobacteria and Its Implications for Gliding Motility

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Oscillin, an extracellular, Ca²⁺‐binding glycoprotein essential for the gliding motility of cyanobacteria