Isolation and Chemical Analysis of the Sheaths of the Filamentous Cyanobacteria Calothrix parietina and C. scopulorum

Weckesser, Jürgen; Hofmann, K. A.; Jürgens, Uwe J.; Whitton, Brian A.; Raffelsberger, Bernd

doi:10.1099/00221287-134-3-629

Cited by 22 publications

(27 citation statements)

References 16 publications

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“…Superficially, the sheath of SP-6 is structurally and chemically similar to sheaths of S. natans (30,45) and cyanobacteria (4,31,43,47,56). The sheaths of these bacteria have all been reported to be composed of a random meshwork of fibrils that are rich in carbohydrate with lesser amounts of protein.…”

Section: Discussionmentioning

confidence: 88%

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Ultrastructure and chemical composition of the sheath of Leptothrix discophora SP-6

1993

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Light microscopy and transmission electron microscopy of thin sections and metal-shadowed specimens showed that the sheath of Leptothrix discophora SP-6 (ATCC 51168) is a tube-like extracellular polymeric structure consisting of a condensed fabric of 6.5-nm-diameter fibrils underlying a more diffuse outer capsular layer. In thin sections, outer membrane bridges seen to contact the inner sheath layer suggested that the sheath fabric was attached to the outer layer of the gram-negative cell wall. The capsular polymers showed an affinity for cationic colloidal iron and polycationic ferritin, indicating that they carry a negative charge. Cell-free sheaths were isolated by treatment with a mixture of lysozyme, EDTA, and N-lauroylsarcosine (Sarkosyl) or sodium dodecyl sulfate (SDS). Both Sarkosyl-and SDS-isolated sheaths were indistinguishable in microscopic appearance. However, the Mn-oxidizing activity of Sarkosyl-isolated sheaths was more stable than that of SDS-isolated sheaths. The Sarkosyl-isolated sheaths also contained more 2-keto-3-deoxyoctanoic acid and more outer membrane protein than SDS-isolated sheaths. The oven-dried mass of detergent-isolated sheaths represented approximately 9% of the total oven-dried biomass of SP-6 cultures; the oven-dried sheaths contained 38% C, 6.9%o N, 6% H, and 2.1% S and approximately 34 to 35% carbohydrate (polysaccharide), 23 to 25% protein, 8% lipid, and 4% inorganic ash. Gas-liquid chromatography showed that the polysaccharide was an approximately 1:1 mixture of uronic acids (glucuronic, galacturonic, and mannuronic acids and at least one other unidentified uronic acid) and an amino sugar (galactosamine). Neutral sugars were not detected.Amino acid analysis showed that sheath proteins were enriched in cysteine (6 mol%). The cysteine residues in the sheath proteins probably provide sulfhydryls for disulfide bonds that play an important role in maintaining the structural integrity of the sheath (D. Emerson and W. C. Ghiorse, J. Bacteriol. 175:7819-7827, 1993 (24,36,39).Leptothrix spp. are similar in physiology and cellular structure to closely related gram-negative aerobic heterotrophic pseudomonads (1, 2, 23, 55). Sheath formation and extracellular metal-oxidizing ability are the two major phenotypic criteria distinguishing them from closely related bacteria. The manganese-and iron-oxidizing activities of L. discophora SS-1 (ATCC 43182) are at least partly determined by metal-oxidizing proteins excreted by the cells in association with extracellular polymers (3, 10, 13). Presumably the excreted metaloxidizing proteins are associated with polymers located in the sheath. However, strain SS-1 irreversibly lost the ability to form a sheath soon after it was isolated (2). Recently we reported the isolation and maintenance of a new strain of L. discophora, SP-6 (ATCC 51168) (19). A sheathless variant, strain SP-6(sl) (ATCC 51169), also was isolated. Taxonomic studies (19,57) showed that strains SP-6 and SP-6(sl) are very similar but not identical to strain SS-1.

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Section: Discussionmentioning

confidence: 88%

“…cells inside sheaths are protected from grazing by protozoa (17). Other Previous work has identified a general pattern in the structure and chemistry of the sheaths of Sphaerotilus natans (22,30,45) and a few filamentous cyanobacteria (4,31,43,46,47,56). These bacterial sheaths consist of a meshwork of polysaccharide-and protein-rich fibrils.…”

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Ultrastructure and chemical composition of the sheath of Leptothrix discophora SP-6

1993

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“…The efficiency of cyanobacterial EPS in the removal of metal ions has been discussed previously, with an emphasis on the monosaccharidic composition of the polymer, the isolation of EPS, and the subsequent utilization with removal assays (5,8,21). Although the chemical composition of the sheaths of several cyanobacterial strains has been determined (14,15,32,33,38,39) and the importance of the capsules and RPS in the metal-removal process has been recognized (6), information about the exact contribution of each type of EPSs and/or functional group to the biosorption of the metal is still very limited.…”

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Sheathless Mutant of Cyanobacterium Gloeothece sp. Strain PCC 6909 with Increased Capacity To Remove Copper Ions from Aqueous Solutions

Micheletti

Pereira

Mannelli

et al. 2008

Appl Environ Microbiol

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The cyanobacterium Gloeothece sp. strain PCC 6909 and its sheathless mutant were tested for their abilities to remove copper ions from aqueous solutions, with the aim of defining the role of the various outermost polysaccharidic investments in the removal of the metal ions. Microscopy studies and chemical analyses revealed that, although the mutant does not possess a sheath, it releases large amounts of polysaccharidic material (released exocellular polysaccharides [RPS]) into the culture medium. The RPS of the wild type and the mutant are composed of the same 11 sugars, although they are present in different amounts, and the RPS of the mutant possesses a larger amount of acidic sugars and a smaller amount of deoxysugars than the wild type. Unexpectedly, whole cultures of the mutant were more effective in the removal of the heavy metal than the wild type (46.3 ؎ 3.1 and 26.7 ؎ 1.5 mg of Cu 2؉ removed per g of dry weight, respectively). Moreover, we demonstrated that the contribution of the sheath to the metal-removal capacity of the wild type is scarce and that the RPS of the mutant is more efficient in removing copper. This suggests that the metal ions are preferably bound to the cell wall and to RPS functional groups rather than to the sheath. Therefore, the increased copper binding efficiency observed with the sheathless mutant can be attributed to the release of a polysaccharide containing larger amounts and/or more accessible functional groups (e.g., carboxyl and amide groups).Cyanobacteria are a large and widespread group of photoautotrophic microorganisms that combine the ability to perform an oxygenic plant-like photosynthesis with typical prokaryotic features (40). Outside their atypical gram-negative cell walls (15), many strains possess outermost structures, mainly of a polysaccharidic nature, that differ in thickness and consistency. These structures can be referred to as sheaths, capsules, and slimes (4). The term sheath is applied to the usually thin and electron-dense layer surrounding the cells or the cell groups; the capsule refers to the thick and gelatinous layer intimately associated with the cell surface and presenting sharp outlines, whereas the term slime is used to designate the mucilaginous material that is dispersed around the organism but does not reflect the shape of the cells. During cell growth, aliquots of these polysaccharides can be released into the surrounding medium (referred to as released exocellular polysaccharides [RPS]), causing a progressive increase in its viscosity (4). The cyanobacterial exopolysaccharides (EPSs; a general term which includes both the polysaccharidic structures that remain intimately associated with the cell, i.e., the sheath and capsule, and those released into the culture medium, i.e., the RPS) exhibit some typical characteristics that distinguish them from the polymers synthesized by other bacteria: they frequently contain two different uronic acids, they build a polymer particularly rich in negatively charged groups, they possess a larger number o...

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“…The functions of cyanobacterial exopolymers are many. A coating of extracellular polysaccharides may protect against dehydration (8,17,38) or provide chemically reactive sites capable of protecting the cell proper against detrimental metal uptake or biomineralization (31,38,46). Exopolymers may also protect against predation (8,48) or aid in adhesion to a solid substrate (8,38).…”

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Characterization and Implications of the Cell Surface Reactivity of Calothrix sp. Strain KC97

Phoenix

Martinez

Konhauser

et al. 2002

Appl Environ Microbiol

125

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The cell surface reactivity of the cyanobacterium Calothrix sp. strain KC97, an isolate from the Krisuvik hot spring, Iceland, was investigated in terms of its proton binding behavior and charge characteristics by using acid-base titrations, electrophoretic mobility analysis, and transmission electron microscopy. Analysis of titration data with the linear programming optimization method showed that intact filaments were dominated by surface proton binding sites inferred to be carboxyl groups (acid dissociation constants [pK a ] between 5.0 and 6.2) and amine groups (mean pK a of 8.9). Sheath material isolated by using lysozyme and sodium dodecyl sulfate generated pK a spectra similarly dominated by carboxyls (pK a of 4.6 to 6.1) and amines (pK a of 8.1 to 9.2). In both intact filaments and isolated sheath material, the lower ligand concentrations at mid-pK a values were ascribed to phosphoryl groups. Whole filaments and isolated sheath material displayed total reactive-site densities of 80.3 ؋ 10 ؊5 and 12.3 ؋ 10 ؊5 mol/g (dry mass) of cyanobacteria, respectively, implying that much of the surface reactivity of this microorganism is located on the cell wall and not the sheath. This is corroborated by electrophoretic mobility measurements that showed that the sheath has a net neutral charge at mid-pHs. In contrast, unsheathed cells exhibited a stronger negative-charge characteristic. Additionally, transmission electron microscopy analysis of ultrathin sections stained with heavy metals further demonstrated that most of the reactive binding sites are located upon the cell wall. Thus, the cell surface reactivity of Calothrix sp. strain KC97 can be described as a dual layer composed of a highly reactive cell wall enclosed within a poorly reactive sheath.

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Isolation and Chemical Analysis of the Sheaths of the Filamentous Cyanobacteria Calothrix parietina and C. scopulorum

Cited by 22 publications

References 16 publications

Ultrastructure and chemical composition of the sheath of Leptothrix discophora SP-6

Ultrastructure and chemical composition of the sheath of Leptothrix discophora SP-6

Sheathless Mutant of Cyanobacterium Gloeothece sp. Strain PCC 6909 with Increased Capacity To Remove Copper Ions from Aqueous Solutions

Characterization and Implications of the Cell Surface Reactivity of Calothrix sp. Strain KC97

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