The <i>Azolla, Anabaena azollae</i> Relationship

Peters, Gerald A.; Mayne, Berger C.

doi:10.1104/pp.53.6.813

Cited by 161 publications

(46 citation statements)

References 22 publications

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“…Mature fronds of each strain of Azolla were collected, washed several times with distilled water and the roots were removed. The 'gentle roller' Evolution of symbiosis in nostocacean cyanobacteria procedure (Peters & Mayne, 1974) was utilized to isolate filaments of symbiotic cyanobacteria from within leaf cavities.…”

Section: Methodsmentioning

confidence: 99%

Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria

Papaefthimiou

Hrouzek

Mugnai

et al. 2008

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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Many cyanobacteria commonly identified as belonging to the genus Nostoc are well-known cyanobionts (symbionts) of a wide variety of plants and fungi. They form symbioses with bryophytes, pteridophytes, gymnosperms and angiosperms that are considerably different in the type of reciprocal interaction between the host and the cyanobiont. The phylogenetic and taxonomic relationships among cyanobionts isolated from different hosts and Nostoc strains isolated from free-living conditions are still not well understood. We compared phylogeny and morphology of symbiotic cyanobacteria originating from different host plants (genera Gunnera, Azolla, Cycas, Dioon, Encephalartos, Macrozamia and Anthoceros) with free-living Nostoc isolates originating from different habitats. After preliminary clustering with ARDRA (amplified rDNA restriction analysis), phylogeny was reconstructed on the basis of 16S rRNA gene sequences and compared with morphological characterization, obtaining several supported clusters. Two main Nostoc clusters harboured almost all cyanobionts of Gunnera, Anthoceros and of several cycads, together with free-living strains of the species Nostoc muscorum, Nostoc calcicola, Nostoc edaphicum, Nostoc ellipsosporum and strains related to Nostoc commune. We suggest that the frequent occurrence of symbiotic strains within these clusters is explained by the intensive hormogonia production that was observed in many of the strains studied. However, no evidence for discrimination between symbiotic and free-living strains, either by molecular or morphological approaches, could be found. Sequences of Azolla cyanobiont filaments, taken directly from leaf cavities, clustered tightly with sequences from the planktic cyanobacterium Cylindrospermopsis raciborskii, from the benthic Anabaena cylindrica 133 and from Anabaena oscillarioides HINDAK 1984/43, with high bootstrap values. The phylogenetic analysis showed that two distinct patterns of evolution of symbiotic behaviour might exist for the nostocacean cyanobacteria, one leading to symbioses of Nostoc species with a wide variety of plants, the other leading to the association of a unique cyanobacterial type with the water fern Azolla.

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Section: Methodsmentioning

confidence: 99%

Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria

Papaefthimiou

Hrouzek

Mugnai

et al. 2008

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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“…While nitrogenase is unique to the alga (21) its lability makes it unsuitable for quantitation. Chl a/b ratios provided another estimate, but this was based on the absence of Chl b from the alga (20) and was therefore not as sensitive. A third method, the quantitation of phycobilins which are unique to the alga in the association, was employed.…”

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confidence: 99%

Azolla-Anabaena Relationships

Ray

Peters²,

Toia³

et al. 1978

Plant Physiol.

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The N2-fixing Azolla-Anabaena symbiotic association is characterized in regard to individual host and symbiont contributions to its total chlorophyll, protein, and levels of ammonia-assimilating enzymes. The phycocyanin content of the association and the isolated blue-green algal symbiont was used as a standard for this characterization. Phycocyanin was measured by absorption and fluorescence emission spectroscopy. The phycocyanin content and total phycobilin complement of the symbiotic algae were distinct from those of Anabaena cylindrica and a free-living isolate of the Azoila endophyte. The algal symbiont accounted for less than 20% of the association's chlorophyll and protein. Acetylene reduction rates in the association (based solely on the amount of algal chlorophyll) were 30 to 50% higher than those attained when the symbiont was isolated directly from the fern. More than 75% of the association's glutamate dehydrogenase and glutamine synthetase activities are contributed by the host plant. The specific activity of glutamate dehydrogenase is greater than that of glutamine synthetase in the association and individual partners. Both the host and symbiont have glutamate synthase activity. The net distribution of these enzymes is discussed in regard to the probable roles of the host and symbiont in the assimilation of ammonia resulting from N2 fixation by the symbiont.The Azolla-Anabaena azollae symbiosis is an N2-fixing association between a eukaryotic fern and a prokaryotic alga, both of which exhibit a higher plant type of photosynthesis (18,19).As an approach toward the characterization of the role of the host and symbiont4 in the association, it was considered important to determine the contribution of the partners to the association's Chl, protein, and ammonia-assimilating enzymes. While the alga could be isolated free of the fern, its removal from the host was never complete. Thus it was necessary to find an independent quantitative estimate for the amount of alga in the association. While nitrogenase is unique to the alga (21) its lability makes it unsuitable for quantitation. Chl a/b ratios provided another estimate, but this was based on the absence of Chl b from the alga (20) and was therefore not as sensitive. A third method, the quantitation of phycobilins which are unique to the alga in the association, was employed. A procedure involving fluorescence emission spectroscopy at 77 K permitted quantitative measurement of phycobilins in the association, where the fern's Chl b '

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“…cultures, algal isolation, and chlorophyll determinations were essentially as described previously (10,12). C2H2 Reduction and H2 Evolution.…”

Section: Methodsmentioning

confidence: 99%

“…Azolla is a genus of small aquatic ferns which, under natural conditions, invariably contain the heterocystous blue-green alga, Anabaena azollae, as a symbiont in an enclosed chamber in the dorsal leaf lobes (10,12). In the intact association, the alga can provide the Azolla plant with its total nitrogen requirement.…”

Section: Introductionmentioning

confidence: 99%

“…This ratio decreased with increasing pN2 and the decrease was correlated with less H2 production. Ratios obtained at N2 partial pressures of approximately 0.3, 0.6, and 0.8 atm, respectively, were 3.2, 2.0, and 1.7 for the association and 4.4, 3.0, and 2.5 for the isolated symbiont.Rates obtained for C2H2 reduction, N2 fixation, and H2 production were used to obtain an expression of the electron balance in vivo.Azolla is a genus of small aquatic ferns which, under natural conditions, invariably contain the heterocystous blue-green alga, Anabaena azollae, as a symbiont in an enclosed chamber in the dorsal leaf lobes (10,12). In the intact association, the alga can provide the Azolla plant with its total nitrogen requirement.…”

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Azolla-Anabaena azollae Relationship

Peters

Toia²,

Lough³

1977

Plant Physiol.

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In order to characterize the reactions catalyzed by nitrogenase in the Azolla-Anabaena association, '5N2 fixation, C2H2 reduction, and ATPdependent H2 production were measured in both the Azolla-Anabaena complex and in the alga isolated from the complex.The rate of reduction of substrates and of ATP-dependent H2 evolution was determined at varous partial pressures of C2H2 and N2. A pC2H2 of 0.1 atm was nearly optimal for C2H4 production and inhibited H2 production by 95%. The ratio of C2H2 reduced to N2 fixed was determined as a function of constant pC2H2 (0.1 atm) and variable pN2. This ratio decreased with increasing pN2 and the decrease was correlated with less H2 production. Ratios obtained at N2 partial pressures of approximately 0.3, 0.6, and 0.8 atm, respectively, were 3.2, 2.0, and 1.7 for the association and 4.4, 3.0, and 2.5 for the isolated symbiont.Rates obtained for C2H2 reduction, N2 fixation, and H2 production were used to obtain an expression of the electron balance in vivo.Azolla is a genus of small aquatic ferns which, under natural conditions, invariably contain the heterocystous blue-green alga, Anabaena azollae, as a symbiont in an enclosed chamber in the dorsal leaf lobes (10,12). In the intact association, the alga can provide the Azolla plant with its total nitrogen requirement. Previous studies showed that the symbiont contained nitrogenase and was capable of C2H2 reduction, ATP-dependent H2 evolution, and excretion of ammonia (10,11,13).Although C2H2 reduction is a simple and sensitive assay of nitrogenase activity, C2H2 is not the biologically important substrate, and the assay is an indirect measurement of nitrogen fixation. Since the reduction of N2 to 2NH3 requires six electrons while reduction of C2H2 to C2H4 requires two electrons, a theoretical conversion factor of 3C2H2 reduced per N2 fixed is frequently used in estimating nitrogen fixation from C2H2 reduction assays. Studies on isolated nitrogenase have shown that when provided with a source of ATP and reductant the rate of electron flow through the enzyme is independent of the substrate (7,20). Moreover, while normal assay levels of C2H2 almost totally suppress H2 production, some electrons continue to be utilized in reducing protons to H2 when N2 is the substrate and employed at saturating levels (16,20). Thus, the C2H2/N2 ratio is usually closer to 4 for nitrogenase in vitro. However, in vivo studies have produced a range of ratios from less than 2 to greater than 8 (8), and it would appear that the ratio may be dependent upon both the organism and experimental conditions employed. This is a report on 15N2 fixation by the fern-algal association and the symbiont isolated directly from the leaf cavities. In order to determine whether a specific conversion factor can be used, and to assess some factors capable of affecting it, the effect of pN2 on N2 fixation and ATP-dependent H2 evolution was determined in parallel with measurements of C2H2 reduction. Ratios of C2H2 reduction to N2 fixation and the effect of H2 evoluti...

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The Azolla, Anabaena azollae Relationship

Cited by 161 publications

References 22 publications

Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria

Differential patterns of evolution and distribution of the symbiotic behaviour in nostocacean cyanobacteria

Azolla-Anabaena Relationships

Azolla-Anabaena azollae Relationship

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