Nitrogenase — Hydrogenase interrelationships in Rhizobia

Dixon, R. O. D.

doi:10.1016/s0300-9084(78)80819-0

Cited by 63 publications

(25 citation statements)

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“…Most N2-fixing free-living microorganisms are able to oxidize the H2 produced by the nitrogenase reaction and recapture some of the energy lost through H2 evolution (1,2). Recent experiments in which soybeans were inoculated with otherwise isogenic Hup+ and Hup-Rhizobium japonicum strains indicate a significant increase in plant nitrogen content and total weight when the plants were grown to maturity before harvesting.t However, only a minority of R. japonicum strains possess an active H2 uptake system (3).…”

mentioning

confidence: 99%

Intra- and interspecies transfer and expression of Rhizobium japonicum hydrogen uptake genes and autotrophic growth capability

Lambert

Cantrell

Hanus

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

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Cosmids containing hydrogen uptake genes have previously been isolated in this laboratory. Four new cosmids that contain additional hup gene(s) have now been identified by conjugal transfer of a Rhizobium japonicum 122DES gene bank into a Tn5-generated Hup-mutant and screening for the acquisition ofHup activity. The newly isolated cosmids, pHU50-pHU53, contain part of the previously isolated pHU1 but extend as far as 20 kilobases beyond its border. pHU52 complements five of six Hup-mutants and confers activity on several Hup y wild-tpe R. japonicum strains in the free-living state and where tested in nodules. Transconjugants obtained from interspecies transfer of pHU52 to Rhizobium meliloti 102F28, 102F32, and 102F51 and Rhizobium leguminosarum 128C53 showed hydrogen-dependent methyleneblue reduction, performed the oxyhydrogen reaction, and showed hydrogen-dependent autotrophic growth by virtue of the introduced genes. The identity of the presumptive transconjugants was confirmed by antibiotic-resistance profiles and by plant modulation tests.Hydrogen evolution that accompanies dinitrogen reduction results in an inefficient use of the energy needed for nitrogen fixation. Most N2-fixing free-living microorganisms are able to oxidize the H2 produced by the nitrogenase reaction and recapture some of the energy lost through H2 evolution (1, 2). Recent experiments in which soybeans were inoculated with otherwise isogenic Hup+ and Hup-Rhizobium japonicum strains indicate a significant increase in plant nitrogen content and total weight when the plants were grown to maturity before harvesting.t However, only a minority of R. japonicum strains possess an active H2 uptake system (3). Highly active H2 uptake systems are lacking in Rhizobium meliloti and most other fast-growing rhizobia. A symbiotic plasmid possessing hydrogen uptake genes has been transferred from Rhizobium leguminosarum to R. meliloti (4, t).Cantrell et al. (5) constructed a gene bank of R. japonicum strain 122DES, from which overlapping cosmids containing hydrogen uptake genes were isolated by complementation of the Hup-point mutant PJ17 by using a colony assay (6). However, several observations indicated that more hupspecific DNA remained to be isolated (7).Since hydrogen recycling may be a beneficial trait, it is desirable to transfer hydrogen uptake (hup) genes from R, japonicum to other Hup-rhizobia. Here, we report that a cosmid (pHU52) apparently encoding all essential Hup determinants has been isolated. This cosmid confers Hup activity and autotrophic growth capability to Hup-R. japonicum strains, R. meliloti, and R. leguminosarum. MATERIALS AND METHODSBacterial Strains, Growth Media, and Growth Conditions. Strains of Escherichia coli and R. japonicum used in this study are listed elsewhere (5, 8). E. coli was grown in LB medium (9); rhizobial strains were routinely grown in yeast extract mannitol medium (8). Rhizobia were cultured chemolithotrophically (10, 11) on Repaske's liquid medium (12, 13) with 1.5% Noble agar added for plates. Pr...

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confidence: 99%

Intra- and interspecies transfer and expression of Rhizobium japonicum hydrogen uptake genes and autotrophic growth capability

Lambert

Cantrell

Hanus

et al. 1985

Proc. Natl. Acad. Sci. U.S.A.

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“…This H2 loss results in an inefficient use ofthe energy provided by the organism to the N2-fixing process. Most N2 fixing, freeliving microorganisms, but a minority of strains of Rhizobium, possess the capacity for synthesis ofan H2-recycling system that oxidizes the H2 produced during N2 fixation, thus recapturing some ofthe energy expended during H2 evolution (1,2). Dixon (3) pointed out several potential advantages of H2-oxidizing capability to N2-fixing organisms.…”

mentioning

confidence: 99%

Construction of a Rhizobium japonicum gene bank and use in isolation of a hydrogen uptake gene

Cantrell

Haugland

Evans

1983

Proc. Natl. Acad. Sci. U.S.A.

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“…In terms of overall net photosynthate generated by the plant, these economies were equivalent to 5% and 2% of the carbon utilized in the two periods, respectively. From the differences in H2 evolution and CO2 production by nodules of the two symbloses, the cost of H2 evolution was found to be 3.83 ± 0.6 milimles CO2millimoles H2 for plants grown in sand culture and 1.69 ± 0.48 millmoles COJmillmles H2 for those in water culture.In both symbioses, the ratio of H2 evolution to N2 fixed varied markedly during ontogeny, indicating a significant variation in the relative efficiency and thus metabolic cost of N2 fixation at different stages during development.Concomitant with N2 fixation in legume nodules the enzyme nitrogenase reduces protons to form H2 (7,8, 21). The ratio of H2 produced to N2 fixed has been suggested from studies of the isolated enzyme to occur with a minimum value of 1:1 (14) and it has been proposed that as much as 60%o of the electron flow through nitrogenase in vivo may lead to proton reduction (8, 22).…”

mentioning

confidence: 99%

“…Concomitant with N2 fixation in legume nodules the enzyme nitrogenase reduces protons to form H2 (7,8,21). The ratio of H2 produced to N2 fixed has been suggested from studies of the isolated enzyme to occur with a minimum value of 1:1 (14) and it has been proposed that as much as 60%o of the electron flow through nitrogenase in vivo may lead to proton reduction (8,22).…”

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confidence: 99%

Significance of Hydrogen Evolution in the Carbon and Nitrogen Economy of Nodulated Cowpea

Rainbird¹,

Atkins²,

Pate³

et al. 1983

Plant Physiol.

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The carbon and nitrogen economies of a single cultivar of cowpea ( Vigna unguicuadta (L.) Walp. cv Caloona) nodulated with either a high H2-evolving strain (176A27) or a low H2-evolving strain (CB756) of Rhizobiwm were compared. The two symbioses did not differ in total dry matter production, seed yield, nitrogen fixed, the spectrum of nitrogenous solutes produced by nodules for export, or the partitioning of net photosynthate within the plant throughout the growth cycle. Detailed examination of the carbon and nitrogen economy of the nodules, however, showed a significant difference between the symbioses. Nodules formed with CB756 lost less CO2 in respiration compared to the higher R2-evolving symbioses and this could have been largely responsible for a 36% better economy of carbon use in CB756 nodules during the period of maximum H2 evolution (48-76 days) and over the whole growth period (20-90 days), a 16% economy. In terms of overall net photosynthate generated by the plant, these economies were equivalent to 5% and 2% of the carbon utilized in the two periods, respectively. From the differences in H2 evolution and CO2 production by nodules of the two symbloses, the cost of H2 evolution was found to be 3.83 ± 0.6 milimles CO2millimoles H2 for plants grown in sand culture and 1.69 ± 0.48 millmoles COJmillmles H2 for those in water culture.In both symbioses, the ratio of H2 evolution to N2 fixed varied markedly during ontogeny, indicating a significant variation in the relative efficiency and thus metabolic cost of N2 fixation at different stages during development.Concomitant with N2 fixation in legume nodules the enzyme nitrogenase reduces protons to form H2 (7,8, 21). The ratio of H2 produced to N2 fixed has been suggested from studies of the isolated enzyme to occur with a minimum value of 1:1 (14) and it has been proposed that as much as 60%o of the electron flow through nitrogenase in vivo may lead to proton reduction (8, 22). Since nodule functioning is apparently closely dependent on the availability of photosynthate (10) expended by nitrogenase.Significantly greater dry matter yield and N2 fixation under growth cabinet conditions has been shown by a number ofsoybean symbioses formed with Rhizobium strains able to recycle H2 compared to those formed with strains unable to oxidize H2 (1). While the Rhizobium strains used could have differed in many traits as well as hydrogenase and, under field conditions, yield response to the character was not significant (9), these studies indicate that H2 recycling in nodules may indeed enhance the efficiency of photosynthate use in legumes.In this study, the detailed carbon and nitrogen economies of a single cowpea variety ( Vigna unguiculata (L.) Walp. cv Caloona) nodulated either with a strain ofRhizobium resulting in a low level (CB756) or a high level (176A27) of H2 evolution in the symbioses have been compared. Particular emphasis has been placed on the relative costs of N2 fixation in the economy of carbon use in nodules of the two symbioses and in the...

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Nitrogenase — Hydrogenase interrelationships in Rhizobia

Cited by 63 publications

References 10 publications

Intra- and interspecies transfer and expression of Rhizobium japonicum hydrogen uptake genes and autotrophic growth capability

Intra- and interspecies transfer and expression of Rhizobium japonicum hydrogen uptake genes and autotrophic growth capability

Construction of a Rhizobium japonicum gene bank and use in isolation of a hydrogen uptake gene

Significance of Hydrogen Evolution in the Carbon and Nitrogen Economy of Nodulated Cowpea

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