Evidence for protection of nitrogenase from O2 by colony structure in the aerobic diazotroph Gluconacetobacter diazotrophicus

Dong, Zhibao; Zelmer, C. D.; Canny, M. J.; McCully, M. E.; Luit, B. van; Pan, Bo; Faustino, Randolph S.; Pierce, Grant N.; Vessey, J. Kevin

doi:10.1099/00221287-148-8-2293

Cited by 24 publications

(13 citation statements)

References 21 publications

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“…It secretes an enzyme, levansucrase, which hydrolyses sucrose and catalyses the formation of the exopolysaccharide fructan levan [57] 1 which limits oxygen diffusion. This protects nitrogenase activity from excessive oxygen flux, enabling the bacteria to fix nitrogen even if the pO 2 is not much lower than tropospheric levels [58]. Detoxification of reactive oxygen species may also occur [59].…”

Section: Nitrogen Fixation In Sugarcanementioning

confidence: 99%

Establishing symbiotic nitrogen fixation in cereals and other non-legume crops: The Greener Nitrogen Revolution

Dent

Cocking

2017

Agric & Food Secur

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Haber's invention of the synthesis of ammonia from its elements is one of the cornerstones of modern civilization. For nearly a century, agriculture has come to rely on synthetic nitrogen fertilizers produced from ammonia. This largescale production is now supporting nearly half of the world's population through increased food production. But whilst the use of synthetic nitrogen fertilizers brought enormous benefits, including those of the Green Revolution, the world needs to disengage from our ever-increasing reliance on nitrogen fertilizers produced from fossil fuels. Their pollution of the atmosphere and water systems has become a major global environmental and economic concern. Naturally, legume crops such as peas and beans can fix nitrogen symbiotically by interacting with soil nitrogen-fixing rhizobia, bacteria that become established intracellularly within root nodules. Ever since this was first demonstrated in 1888, consistent attempts have been made to extend the symbiotic interaction of legumes with nitrogen-fixing bacteria to non-legume crops, particularly cereals. In 1988, a fresh impetus arose from the discovery of Gluconacetobacter diazotrophicus (Gd), a non-nodulating, non-rhizobial, nitrogen-fixing bacterium isolated from the intercellular juice of sugarcane. Subsequently, strains of Gd inoculated under specific conditions were shown to intracellularly colonize the roots and shoots of the cereals: wheat, maize (corn) and rice, as well as crops as diverse as potato, tea, oilseed rape, grass and tomato. An extensive field trials programme using a seed inoculum technology based on Gd (NFix ® ) indicates that NFix ® is able to significantly improve yields of wheat, maize, oilseed rape and grasses, in both the presence and absence of synthetic nitrogen fertilizers. Evidence suggests that these benefits are accruing through a possible combination of intracellular symbiotic nitrogen fixation, enhanced rates of photosynthesis and the presence of additional plant growth factors. Here, we discuss the research events that have led to this important development and present results demonstrating the efficacy of NFix ® technology in non-legume crops, in particular cereals.

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Section: Nitrogen Fixation In Sugarcanementioning

confidence: 99%

Establishing symbiotic nitrogen fixation in cereals and other non-legume crops: The Greener Nitrogen Revolution

Dent

Cocking

2017

Agric & Food Secur

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“…Secondly, the fructo-oligosaccharide levan; this enables an unusual feature of G. diazotrophicus, namely its ability to fix nitrogen in colonies grown on both semi-solid and solid media [124][125][126]. This is achieved because of the levan mucilage in culture, is capable of limiting oxygen diffusion.…”

Section: Nitrogen Fixation In G Diazotrophicusmentioning

confidence: 99%

“…There is some evidence for a nitrogenase protection mechanism in fluctuating levels of oxygen [126], possibly involving a putative FeSII Shethna protein, which forms a complex with the nitrogenase during sudden increases in oxygen pressure. This process renders the enzyme temporarily inactive but protected from oxygen damage, similar to the situation in the species, Azotobacter vinelandii [130].…”

Section: Nitrogen Fixation In G Diazotrophicusmentioning

confidence: 99%

Non-nodular Endophytic Bacterial Symbiosis and the Nitrogen Fixation of Gluconacetobacter diazotrophicus

Dent¹

2018

Symbiosis

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There is a need to reduce the negative polluting influence of mineral nitrogen fertilizers and to develop a more sustainable climate smart agriculture capable of meeting our future food security needs. Biological nitrogen fixation can have a role in this if it can be applied to the major food crop plants. Certain strains of the obligate nitrogen-fixing bacterial endophyte Gluconacetobacter diazotrophicus have the necessary attributes for this role. An 'extra-ordinary endophyte' this bacterium is one of relatively few that has mechanisms to cope with high levels of sucrose, an acidic pH, a wide range of oxygen environments, nitrogen fixation, as well as having respiratory chain attributes that make it a possible candidate eukaryote proto-mitochondria. Having a small genome relative to other endophytes, it is typical of facultative intracellular colonizers, with a life cycle that involves horizontal transfer to other high sucrose species via insects and potential vertical transfer through seeds. Every method used for demonstrating nitrogen fixation in rhizobia have been used to demonstrate nitrogen fixation in G. diazotrophicus both in vitro and in planta, and field trials demonstrate yield increases and the potential to reduce nitrogen fertilizer use, meeting both food security and climate smart agriculture needs.

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“…Subtle adjustments in the composition and functioning of the respiratory chain, mainly differential expression of cytochromes, were described [9-11]. Additionally, diazotrophs grown in air secrete abundant extracellular polysaccharides and live inside colonies that help to produce a local microaerobic environment [12,13]. …”

Section: Introductionmentioning

confidence: 99%

Unraveling the molecular mechanisms of nitrogenase conformational protection against oxygen in diazotrophic bacteria

et al. 2010

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BackgroundG. diazotrophicus and A. vinelandii are aerobic nitrogen-fixing bacteria. Although oxygen is essential for the survival of these organisms, it irreversibly inhibits nitrogenase, the complex responsible for nitrogen fixation. Both microorganisms deal with this paradox through compensatory mechanisms. In A. vinelandii a conformational protection mechanism occurs through the interaction between the nitrogenase complex and the FeSII protein. Previous studies suggested the existence of a similar system in G. diazotrophicus, but the putative protein involved was not yet described. This study intends to identify the protein coding gene in the recently sequenced genome of G. diazotrophicus and also provide detailed structural information of nitrogenase conformational protection in both organisms.ResultsGenomic analysis of G. diazotrophicus sequences revealed a protein coding ORF (Gdia0615) enclosing a conserved “fer2” domain, typical of the ferredoxin family and found in A. vinelandii FeSII. Comparative models of both FeSII and Gdia0615 disclosed a conserved beta-grasp fold. Cysteine residues that coordinate the 2[Fe-S] cluster are in conserved positions towards the metallocluster. Analysis of solvent accessible residues and electrostatic surfaces unveiled an hydrophobic dimerization interface. Dimers assembled by molecular docking presented a stable behaviour and a proper accommodation of regions possibly involved in binding of FeSII to nitrogenase throughout molecular dynamics simulations in aqueous solution. Molecular modeling of the nitrogenase complex of G. diazotrophicus was performed and models were compared to the crystal structure of A. vinelandii nitrogenase. Docking experiments of FeSII and Gdia0615 with its corresponding nitrogenase complex pointed out in both systems a putative binding site presenting shape and charge complementarities at the Fe-protein/MoFe-protein complex interface.ConclusionsThe identification of the putative FeSII coding gene in G. diazotrophicus genome represents a large step towards the understanding of the conformational protection mechanism of nitrogenase against oxygen. In addition, this is the first study regarding the structural complementarities of FeSII-nitrogenase interactions in diazotrophic bacteria. The combination of bioinformatic tools for genome analysis, comparative protein modeling, docking calculations and molecular dynamics provided a powerful strategy for the elucidation of molecular mechanisms and structural features of FeSII-nitrogenase interaction.

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Evidence for protection of nitrogenase from O2 by colony structure in the aerobic diazotroph Gluconacetobacter diazotrophicus

Cited by 24 publications

References 21 publications

Establishing symbiotic nitrogen fixation in cereals and other non-legume crops: The Greener Nitrogen Revolution

Establishing symbiotic nitrogen fixation in cereals and other non-legume crops: The Greener Nitrogen Revolution

Non-nodular Endophytic Bacterial Symbiosis and the Nitrogen Fixation of Gluconacetobacter diazotrophicus

Unraveling the molecular mechanisms of nitrogenase conformational protection against oxygen in diazotrophic bacteria

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