Nitrogen Fixation at the Millennium

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The turn of the millennium from the twentieth to the twenty-first century provides an occasion to review our understanding of a biological process, biological nitrogen fixation, that is of prime importance for the continued survival of mankind. This process has provided a basis for maintaining soil fertility since the beginning of organised agriculture, yet its very existence was confirmed only just over a century ago.

In the intervening years, an enormous intellectual effort has dispersed much of the mystery surrounding biological nitrogen fixation. Biological fixation is widely exploited in agriculture, as are nitrogen fertilisers prepared for the last hundred years under extreme conditions of temperature and pressure. However, despite all our efforts, the fundamental nature of the reactions involved at the heart of the biological process remain unknown. This book aims to describe what we have learned in the last one hundred years or so about biological nitrogen fixation, about what its chemistry appears to be, and how it is applied in agriculture.

This ambitious objective has not been attempted recently. It is aimed at students and those who wish to enter these very challenging areas of research, and who need to learn the state of the art at the turn of the millennium. The authors are all acknowledged world experts in their fields. They have prepared concise, well referenced and authoritative accounts of their subjects.

This book provides a unique summary of the current state of knowledge that will be indispensable to all students and researchers, actual and potential, interested in biological nitrogen fixation. Newton Introduction 1 3 N2-fixing organisms 4 2 Symbiotic associations 4 1 Associative symbioses 5 1 Associations with animals 6 1 Free-living N2-fixing bacteria 6 1 Nitrogenases 6 11 Molybdenum nitrogenase Mo-nitrogenase 7 3 Alternative nitrogenases 10 1 Streptomyces thermoautotrophicus 11 1 nitrogenase Mechanism of nitrogenase action 12 3 Role of MgATP in nitrogenase catalysis 15 1 Electron transport to nitrogenase 16 1 Site-directed mutagenesis applied to 17 1 nitrogenase Nitrogen-fixation nif genes 17 5 Nitrogen-fixation gene cluster 18 1 Proposed functions for the nif-gene 18 3 products NifA-NifL regulatory system 21 1 Chemical systems 22 4 Reactivity models -- in non-aqueous 22 2 systems Reactivity models -- in aqueous solution 24 1 Structural models 25 1 Summary and outlook 26 1 References 27 8 Nitrogenase Structure 35 38 Paul M.

Benton Sanchayita Sen John W. Rubio Paul W. Mayer Patricia dos Santos Lance C. Seefeldt Dennis R. Dean Introduction 1 Background 5 Insight into the effects of amino acid 3 substitutions around the FeMo-cofactor on substrate reduction Rationale and strategy for isolation of an 3 acetylene-resistant MoFe protein Expanding the capacity of nitrogenase to 2 reduce longer-chain alkynes Acetylene interaction with the MoFe protein 1 in the resting state Summary and outlook 1 Acknowledgements 1 References 3 Regulation of Mo Nitrogenases 12 P.

Rudnick C. Under greenhouse conditions as well, no significant yield differences were observed when the plants were grown on dinitrogen versus nitrate as a nitrogen source Gibson, This indicates that legumes using BNF rather than nitrate nitrogen suffer no obvious yield penalties. Urea and ammonium sulfate are normally used to fertilize rice. An important point to note here is that in spite of the greater energy requirement for nitrate assimilation compared to ammonia assimilation , rice yields are better when grown on nitrate combined with ammonia as compared to ammonia alone Xiaoe and Xi, ; Ancheng et al.

The fact that no yield penalty exists for rice grown on nitrate and ammonia rather than ammonia alone suggests that energy may not be limiting.

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The ability of plants to compensate for extra energy consumption cannot be ignored, as photosynthetic systems saturate at relatively low light intensity. Nevertheless, since source and sink metabolisms are tightly coupled, it is reasonable to assume that the extra energy consumption by roots would stimulate the production of biomass in shoots. It is well established that equilibrium between photosynthetic sugar synthesis in the chloroplast-containing leaf cells source tissues and sugar consumption by roots, fruits and grains sink tissues must be maintained for sustaining plant growth and survival.

In plants under optimal light and at the normal carbon dioxide levels, sink limitation occurs when the rate of photosynthesis is limited by insufficient withdrawal of photosynthetic products generated in the green tissues through the Calvin—Benson cycle Sawada et al. It is intuitively envisaged that a nitrogen-fixing symbiosis in rice may be such a strong sink for photosynthate that yields would be impacted. Also, incidentally, in rice the actual grain yields are considerably lower than their maximum genetic potential.

Therefore, in planta nitrogen-fixing attribute may not significantly impact the present yield levels Ladha and Reddy, There has been a biotechnological interest to promote associative nitrogen fixation in non-legume crops that normally use large amounts of chemical fertilizers. Different nitrogen-fixing bacteria have been isolated from cereal roots by culture-dependent methods, and when used as plant inoculants they have varying degrees and strategies for plant growth promotion Kennedy et al. Some past efforts to increase nitrogen fixation in cereals by promoting pseudonodules with phytohormones failed.

Notably, recently obtained ammonium excreting mutants of some plant-associated diazotrophs were effective for promoting plant growth suggesting that they became capable of supplying nitrogen to their hosts.

Nitrogen Fixation at the Millennium

Even though achieving genetically-modified nitrogen-fixing cereal crops is a complex process, the approaches that are being pursued at present are creating exciting possibilities for generating such plants in the foreseeable future. If so, the global environmental benefits of a reduced chemical fertilizer usage will be large, and we suppose that detrimental ecological consequences of nitrogen fixing cereals will be minimal.

Besides nitrogen, other agricultural inputs, such as phosphorus and water, may limit crop productivity. Mycorrhiza and plant cultivars with high phosphate use efficiency should be considered when developing nitrogen fixing cereals. However, we consider that not only the use of microbes and genetically modified plants will be required to achieve this goal, but a better crop management and efficient programs to control human population-growth are needed as well. JM-R contributed to the discussion, searched for references, and corrected the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. National Center for Biotechnology Information , U. Journal List Front Microbiol v. Front Microbiol. Published online Aug 9. Marco A. Julio C. Pallavolu M. Author information Article notes Copyright and License information Disclaimer.

This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology. Received Mar 31; Accepted Jul The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

This article has been cited by other articles in PMC. Abstract Cereals such as maize, rice, wheat and sorghum are the most important crops for human nutrition. Keywords: rice, corn, wheat, sorghum, diazotrophic bacteria, root colonization, Rhizobium , Burkholderia. Introduction Cereals are grasses from the Poaceae family that were domesticated several thousand years ago in different geographical regions in order to take advantage of the edible components of their grain. Sources of Diazotrophic Bacteria Bacteria can get on to the plants either by root colonization from soil carryover, leaf litter Pfeiffer et al.

Open in a separate window. Culture-Independent Identification of Diazotrophs in Cereals By using a culture-independent approach, a better representation of existing diazotrophs may be obtained while the analysis of nifH transcripts has provided results on active diazotrophs. Diazotrophs May Be Human Pathogens It is not uncommon to isolate human or plant pathogens from plants and in many cases they are efficient growth promoting bacteria. Plants as Determinants of Bacterial Interactions Nitrogen fixation is highly variable depending on the associated diazotroph and the plant variety, but the host plant exerts a determinant effect by supplying the carbon and energy source for bacterial growth and nitrogen fixation.

Prospects for Engineering Cereal Plants Besides using associated bacteria to provide nitrogen to cereals other strategies involving the genetic modification of plants have been considered and are reviewed here.

Conclusion and Perspectives There has been a biotechnological interest to promote associative nitrogen fixation in non-legume crops that normally use large amounts of chemical fertilizers. Conflict of Interest Statement The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments We thank Michael Dunn for reading the manuscript. Footnotes Funding. References Abel C. Evaluation of Peruvian maize for resistance to European corn borer Lepidoptera: Pyralidae leaf feeding and ovipositional preference. May photoinhibition be a consequence, rather than a cause, of limited plant productivity? Principles of Seed Pathology. Expression of 16 nitrogenase proteins within the plant mitochondrial matrix. Plant Sci. Metabolic engineering of a diazotrophic bacterium improves ammonium release and biofertilization of plants and microalgae.

Effect of nitrogen NH 4 NO 3 supply on absorption of ammonium and nitrate by conventional and hybrid rice during reproductive growth. Plant Soil 15 — Abiotic factors shape microbial diversity in Sonoran Desert soils. Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLoS One 9 : e An environment friendly engineered Azotobacter can replace substantial amount of urea fertilizer and yet sustain same wheat yield.

Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Soils 30 — Plant responses to bacterial quorum sensing signals. Plant Biol. Future prospects for cereals that fix nitrogen. Science — Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. Soil Biol. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria.

Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17 — Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.

Nature 91— Structure and functions of the bacterial microbiota of plants. State of the art in eukaryotic nitrogenase engineering. FEMS Microbiol. Formation of nitrogenase NifDK tetramers in the mitochondria of Saccharomyces cerevisiae. ACS Synth. Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics 15 : Rhizosphere microbial community structure at different maize plant growth stages and root locations.

Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Rhizosphere microbiome assemblage is affected by plant development. ISME J. Uncultured bacterial diversity in tropical maize Zea mays L. Basic Microbiol. Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. The diversity of archaea and bacteria in association with the roots of Zea mays L. Isolation and characterization of culturable seed-associated bacterial endophytes from gnotobiotically grown Marama bean seedlings.

Associative N 2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant Soil — Diversity of nifH gene pools in the rhizosphere of two cultivars of sorghum Sorghum bicolor treated with contrasting levels of nitrogen fertilizer. Bruijn F. Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Challenges to develop nitrogen-fixing cereals by direct nif -gene transfer. Plant Sci — Soil type and maize cultivar affect the genetic diversity of maize root—associated Burkholderia cepacia populations.

Genome sequences of Klebsiella variicola isolates from dairy animals with bovine mastitis from Newfoundland, Canada. Genome Announc. Tracing the evolutionary path to nitrogen-fixing crops. Wheat seeds promoters harbour bacterial endophytes with potential as plant growth of biocontrol agents Fusarium graminearum.

Expression of nitrogenase gene nifH in roots and stems of rice, Oryza sativa , by endophytic nitrogen-fixing communities. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. Preferential occurrence of diazotrophic endophytes, Azoarcus spp. How a century of ammonia synthesis changed the world. Phylogenetics analysis of Burkholderia species by multilocus sequence analysis. Burkholderia cepacia complex: distribution of genomovars among isolates from the maize rhizosphere in Italy.

Molecular characterization of the diazotrophic bacterial community in uninoculated and inoculated field-grown sugarcane Saccharum sp. Plant Soil 83— Complete genome sequence of the N 2 -fixing broad host range endophyte Klebsiella pneumoniae and virulence predictions verified in mice. PLoS Genet. Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X Microbially mediated plant functional traits. Microbial diversity inside pumpkins: microhabitat-specific communities display a high antagonistic potential against phytopathogens.

Ecol 63 — Use of plant colonizing bacteria as chassis for transfer of N2-fixation to cereals. Polyphasic taxonomy in the genus Burkholderia leading to an amended description of the genus and proposition of Burkholderia vietnamiensis sp. Bacterial diversity of the rhizosphere of maize Zea mays grown in tropical soil studied by temperature gradient gel electrophoresis. Multiresistance genes of Rhizobium etli CFN Plant Microbe Interact.

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PLoS One 7 : e Plant-driven selection of microbes. Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Ecological perspectives on microbes involved in N-cycling. Microbes Environ. Expression of active subunit of nitrogenase via integration into plant organelle genome. PLoS One 11 : e Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z Impact of swapping soils on the endophytic bacterial communities of pre-domesticated, ancient and modern maize.

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Extension of nitrogen fixation to rice - Necessity and possibilities. Geo J. Makati: International Rice Research Institute, , — Plant Microbiome. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Functional potential of soil microbial communities in the maize rhizosphere.

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Inner plant values: diversity, colonization and benefits from endophytic bacteria. Isolation and molecular identification of endophytic diazotrophs from seeds stems of three cereal crops. PLoS One 12 : e Isolation, taxonomic analysis, and phenotypic characterization of bacterial endophytes present in alfalfa Medicago sativa seeds. Expression of a functional oxygen-labile nitrogenase component in the mitochondrial matrix of aerobically grown yeast. Defining the core Arabidopsis thaliana root microbiome. Nature 86— Substrate flow in the rhizosphere.

Plant Soil 1— Enterobacter cloacae , an obligatory endophyte of pollen grains of Mediterranean pines. Folia Microbiol. Evolution of root endosymbiosis with bacteria: How novel are nodules? Trends Plant Sci. Diazotrophic diversity, nifH gene expression and nitrogenase activity in a rice paddy field in Fujian, China.

How are gene sequence analyses modifying bacterial taxonomy? The case of Klebsiella. Diazotrophic bacteria associated with banana Musa spp. Plant Soil 35— Klebsiella variicola and Klebsiella quasipneumoniae with capacity to adapt to clinical and plant settings. Draft genome sequences of Klebsiella variicola plant isolates. Potential use of rhizobial bacteria as promoters of plant growth for increased yield in landraces of African cereal crops.

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Purchase Nitrogen Fixation at the Millennium - 1st Edition. Print Book & E-Book. ISBN , The turn of the millennium from the twentieth to the twenty-first century Biological fixation is widely exploited in agriculture, as are nitrogen.

African J. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. A New approach to modify plant microbiomes and traits by introducing beneficial bacteria at flowering into progeny seeds.

A two-partner secretion system is involved in seed and root colonization and iron uptake by Pseudomonas putida KT The black queen hypothesis: evolution of dependencies through adaptive gene loss. Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Natural association of Gluconacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice.

The development of Azospirillum as a commercial inoculant for improving crop yields. Bacterial flora of endophytes in the maturing seed of cultivated rice Oryza sativa.

Molecular Biology and Genetic Engineering in Nitrogen Fixation

Berlin: Springer-Verlag; , — RNA-seq transcriptional profiling of Herbaspirillum seropedicae colonizing wheat Triticum aestivum roots. Plant Mol. Isoflavonoid-inducible resistance to the phytoalexin glyceollin in soybean rhizobia. Economy of carbon and nitrogen in a nodulated and non-nodulated NO 3 -grown legume. Plant Physiol. Sink regulation of photosynthesis. Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grass.

PLoS Gentet. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Genomic studies of nitrogen-fixing rhizobial strains from Phaseolus vulgaris seeds and nodules. BMC Genomics 17 : Analysis of the bacterial diversity associated with the roots of maize Zea mays L. ISRN Ecol. Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Leaf litter is the main driver for changes in bacterial community structures in the rhizosphere of ash and beech. Soil Ecol. Rhizosphere microbiomes of potato cultivated in the High Andes show stable and dynamic core microbiomes with different responses to plant development.

Agronomic evaluation of non-nodulating and hypernodulating mutants of soybean. Crop Sci. Comparative study of endophytic and endophytic diazotrophic bacterial communities across rice landraces grown in the highlands of northern Thailand. Yield trends are insufficient to double global crop production by PLoS One 8 : e Hyderabad: Society for Advancement of Rice Research; , — Leigh G. Amsterdam: Elsevier; , — Azoarcus spp. Plant Soil 57—