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Hydrogen production by nitrogenase as a potential crop rotation benefit

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Abstract

Both climate change and the adverse effects of chemical use on human and environmental health are recognized as serious issues of global concern. Nowhere is this more apparent than in the agricultural sector where release of greenhouse gases such as carbon dioxide, nitrous oxide and methane continues to be problematic and where use of nitrogen fertilizer is responsible for negative impacts on both human populations and ecosystems. The manipulation of biological nitrogen fixation (BNF) could help alleviate part of the difficulty by decreasing the need for nitrogen fertilizers, which require huge quantities of fossil fuel to produce and contribute to the release of nitrous oxide from soil as well as being responsible for the contamination of drinking water systems and natural habitats. BNF is performed by a variety of microorganisms. One of the most studied examples is the BNF carried out by rhizobial bacteria in symbiosis with their plant hosts such as pea and soybean. Hydrogen gas is an energy-rich, obligate by-product of BNF. Legume symbioses with rhizobia lacking hydrogenase enzymes (which can recycle hydrogen) have traditionally been viewed as energetically inefficient. However, recent studies suggest hydrogen release to soil may be beneficial, increasing soil carbon sequestration and promoting growth of hydrogen-oxidizing bacteria beneficial to plant growth; the alleged superiority of symbiotic performance in rhizobia possessing functional hydrogenases (HUP+) over those rhizobia without functional hydrogenases (HUP−) has also not been conclusively shown. The structure of the iron-molybdenum cofactor or FeMo-co of nitrogenase (the active site of the enzyme) has been elucidated through X-ray crystallography but the mechanism of nitrogen fixation remains unknown. However, studies of effects of hydrogen production on BNF have revealed potential candidate intermediates involved in the nitrogenase reaction pathway and have also shown the role of hydrogen as a competitive inhibitor of N2, with hydrogen now considered to be the primary regulator of the nitrogenase electron allocation coefficient. The regulation of oxygen levels within legume root nodules is also being investigated; nitrogen fixation is energetically expensive, requiring a plentiful oxygen supply but too high an oxygen concentration can irreversibly damage nitrogenase, so some regulation is needed. There is evidence from gas diffusion studies suggesting the presence of a diffusion barrier in nodules; leghaemoglobin is another potential O2 regulator. Possible functions of hydrogenases include hydrogen recycling, protection of nitrogenase from damaging O2 levels and prevention of inhibitory H2 accumulation; there is evidence for H2 recycling only in studies where H2 uptake has been strongly coupled to ATP production and where this is not the case, it is believed that the hydrogenase acts as an O2 scavenger, lowering O2 concentrations. The distribution of hydrogenases in temperate legumes has been found to be narrow and root and shoot grafting experiments suggest the host plant may exert some influence on the expression of hydrogenase (HUP) genes in rhizobia that possess them. Many still believe that HUP+ rhizobia are superior in performance to HUP− species; to this end, many attempts to increase the relative efficiency of nitrogenase through the introduction of HUP genes into the plasmids or chromosomes of HUP− rhizobia have been carried out and some have met with success but many other studies have not revealed an increase in symbiotic performance after successful insertion of HUP genes so the role of HUP in increasing parameters such as N2 fixation and plant yield is still unclear. One advantage of the hydrogen production innate to BNF is that the H2 evolved can be used to measure N2 fixation using new open-flow gas chamber techniques seen as superior to the traditional acetylene reduction assay (ARA) conducted in closed chambers, although H2 cannot be used for field studies yet as the ARA can. However, the ARA is now believed to be unreliable in field studies and it is recommended that other measures such as dry weight, yield and total nitrogen content are more accurate, especially in determining real food production, particularly in the developing nations. Another potential benefit of H2 release from root nodules is that it stays in the soil and has been found to be consumed by H2-oxidizing bacteria, many of which show plant growth–promoting properties such as the inhibition of ethylene biosynthesis in the host plant, leading to root elongation and increased plant growth; they may well be promising as biofertilizers if they can be successfully developed into seed inoculants for non-leguminous crop species, decreasing the need for chemical fertilizers. It has been suggested that rhizobia can produce nitrous oxide through denitrification but this has never been shown; it is possible that hydrogen release may provide more ideal conditions for denitrifying, free-living bacteria and so increase production of nitrous oxide that way and this issue will require more study. However, it seems unlikely that a natural system would release nitrous oxide to the same degree that chemical fertilizers have been shown to do.

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Abbreviations

Abiotic:

Non-living chemical and physical environmental factors such as temperature

ACC:

1-Aminocyclopropane-1-carboxylate, a precursor of ethylene

Acid:

Any chemical compound that when dissolved in water gives a solution with a greater hydrogen ion (H+) activity than that of pure water, thus possessing a pH of less than 7.0

ADP:

Adenosine diphosphate

ANA:

Apparent nitrogenase activity, measured as the rate of hydrogen evolution in air

Anaerobic:

In the absence of oxygen

Antibiotic:

A substance or compound that kills or inhibits the growth of bacteria; bactericidals kill bacteria whereas bacteriostatic agents inhibit bacterial growth

Apoplastic space:

A free diffusional space outside the plasma membrane in plant cells. In roots, this space is interrupted by the Casparian strip; in other plant cells, it is interrupted by air spaces between the cells and the cuticle

Apoplastic pathway:

Through the cell walls of plant cells

Ar:

Argon gas

ARA:

The acetylene reduction assay, a technique for measuring nitrogenase activity/nitrogen fixation in both laboratory and field studies

Assimilation:

The process of conversion of inorganic compounds to organic compounds available to living organisms to provide energy, for example, nitrogen fixation, photosynthesis and animal digestion; similar to fixation

ATP:

Adenosine triphosphate; the molecular energy currency of living cells used to drive metabolic activities

Autocatalytic reaction:

A reaction where the catalyst and the product are one and the same substance

Base:

Any chemical compound that when dissolved in water gives a solution with a lesser hydrogen ion (H+) activity than that of pure water, thus possessing a pH of more than 7.0

Biomass C:

Carbon derived from living or recently living organisms such as plants/plant matter or microorganisms (live and dead cells)

Biotic:

Relating to, produced by or caused by living organisms

C:

Carbon

C2H2 :

Acetylene

C2H4 :

Ethylene, an important plant hormone involved in many stages of development

cm:

Centimetre

CN− :

Cyanide ion; the addition of an electron or loss of a proton results in the negatively charged ion

CO:

Carbon monoxide

CO2 :

Carbon dioxide, a significant greenhouse gas

Casparian strip:

A band of cell wall material in the radial and transverse walls of the root endodermis that prevents passive diffusion of H2O and solutes into the stele of plant roots

Cofactor:

A non-protein compound bound to a protein (often an enzyme) that is required for the protein’s biological activity

Constitutive:

Always present or active, for example gene products that are always produced, a protein whose activity is constant or defences that are always active as opposed to inducible

Cosmid:

A hybrid plasmid designed to carry more DNA than naturally occurring plasmids; these constructs frequently contain genes for selection such as antibiotic resistance genes and are often used in cloning procedures

D2 :

Deuterium

D2O:

Deuterium oxide or heavy water

Dalton:

Da; a unit of mass used to express atomic or molecular masses; the approximate mass of a hydrogen atom, proton or neutron

DAPI:

4′-6-Diamidino-2-phenylindole, a DNA stain

Denitrification:

This process completes the nitrogen cycle by returning N2 to the atmosphere through the reduction of nitrate (NO3 −). This is carried out primarily by heterotrophic bacteria in hypoxic or anaerobic conditions in the soil, for instance the pseudomonads and Paracoccus denitrificans

Diazotroph:

A prokaryote (microorganism) capable of reducing N2 and using it as an energy source

Diimides:

The azo (–N≡N–) functional group or a compound containing such a group

Dimer:

A dimer is a chemical/biological entity comprised of two similar subunits held together by either intramolecular forces (covalent bonds) or weaker intermolecular forces such as ionic or hydrogen bonds. Homodimers occur where the two subunits are identical, whereas heterodimers occur when the two subunits are not identical

DNA:

Deoxyribonucleic acid; the molecular carrier of genetic information in living organisms

e− :

Electrons; atomic particles that carry a negative electrical charge

EAC:

Electron allocation coefficient; a ratio representing the proportion of electron flow through nitrogenase that works towards the reduction of dinitrogen instead of hydrogen production

ETC:

The electron transport chain; a group of enzyme complexes that moves electrons from electron donors to electron acceptors in a chain of biochemical reactions that produce ATP

Fe:

Iron, a metal element

FeMo-co:

The iron-molybdenum cofactor found within the MoFe protein of the nitrogenase enzyme

FISH:

Fluorescent in situ hybridization; a cytogenetic technique used to detect and localize the presence or absence of specific DNA sequences on chromosomes. It uses fluorescent DNA probes that bind only to sequences with which they share a high degree of similarity. This method is used to reveal spatial and/or temporal gene expression patterns

Fixation:

The fixation of CO2 to organic compounds and the fixation of dinitrogen to ammonia are both examples of fixation and both are also reduction reactions.

Fungicide:

Chemicals or organisms used to kill or inhibit fungi or fungal spores

GEQ:

Gas exchange quotient; a ratio representing proportions of individual gases within a gas mixture and their exchange rates under dynamic conditions

H+ :

Protons; atomic particles that carry a positive electrical charge, in this case from a hydrogen atom

H2 :

Dihydrogen, a gaseous element

H2O:

Hydrogen oxide or water

ha:

Hectare

HD:

Hydrogen deuteride, a metal hydride

HE assay:

Hydrogen evolution assay; an alternative method for measuring nitrogenase activity/nitrogen fixation. Seen as more accurate than the ARA, it can at present only be used in laboratory studies

HOD:

Hydrogen deuteroxide; a protonated acid residue

HUP:

Hydrogenase uptake enzyme system; the hydrogenase takes up H2 produced during nitrogen fixation and recycles it

HUP− :

Hydrogenase uptake negative; rhizobia possessing either no hydrogenase or a non- or low-functioning hydrogenase enzyme

HUP+ :

Hydrogenase uptake positive; rhizobia possessing a functional hydrogenase enzyme

Hydrazine:

N2H4; an intermediate in the anaerobic oxidation of ammonia and a possible intermediate in the reduction of dinitrogen to ammonia

Hydride:

H−; the negatively charged hydrogen ion

Hypoxic:

Low-oxygen environment

Ionophore:

A lipid-soluble molecule manufactured by microorganisms to transport ions across lipid bilayers of the cell membrane. These can be of two kinds: (a) compounds that bind to an ion and shield its charge as it crosses the hydrophobic interior of the cell’s lipid membrane or (b) channel formers that form hydrophilic pores in lipid membranes and let ions pass through without contacting the cell’s hydrophobic lipid interior. Ionophores disrupt ion concentration gradients across cell membranes, which are required by microorganisms for survival and functionality, and so show antibiotic properties; some microorganisms naturally produce ionophores to compete against other microorganisms

K:

Potassium, a metal element

K+ :

Potassium ion; the removal of an electron results in the positively charged ion

kb:

Kilobases, one thousand base pairs

kDa:

Kilodaltons, one thousand daltons

Km:

The amount of substrate required to reach one half the maximal velocity of a chemical reaction

Kjeldahl method:

A technique to quantitatively determine nitrogen amounts in chemical substances developed by Johan Kjeldahl in 1883. First, a substance is heated with sulphuric acid (H2SO4) which decomposes organic substrate through oxidation and releases reduced nitrogen as ammonium sulphate; the sample decomposition is complete when the very dark medium becomes clear and colourless. This solution is then distilled with sodium hydroxide (NaOH, a strong base) as an ammonium salt and finally as NH3. The amount of NH3 present, which represents the amount of nitrogen present in the sample, is then determined by back filtration with the end of a condenser dipped in boric acid solution. The ammonia reacts with the acid and the remainder of the acid is titrated with sodium bicarbonate (NaCO3) solution with a methyl orange pH indicator. This technique combines universality, precision and reducibility and is internationally recognized as the method for determining food protein content; however, it is not a true measure of protein content as it also measures non-protein nitrogen but it is very accurate for measuring total nitrogen content

L:

Litre; one thousand millilitres

Lb:

Leghaemoglobin; an oxygen-carrying haem protein found within the nitrogen-fixing root nodules of legume plants synthesized by the plant host in response to rhizobial infection. It has a high affinity for O2 and so can deliver enough O2 to rhizobia for respiration but simultaneously buffers concentrations of free O2 in infected plant cells, ensuring that nitrogenases will not be deactivated by excessive O2 concentrations

MDa:

Megadalton; one million daltons

Labile:

Susceptible to change or breakdown. For example, nitrogenase is oxygen labile because in the presence of O2, nitrogenase will be deactivated and irreversibly break down

Mg:

Magnesium, a metal element

Mo:

Molybdenum, a metal element

MRI:

Magnetic resonance imaging; a method that utilizes a powerful magnetic field to align the nuclear magnetization of atoms (often hydrogen atoms). Radio frequency fields are then used to alter the magnetization’s alignment, causing the atoms’ nuclei to generate a rotating magnetic field that can be detected by scanners. Most familiar as a medical imaging technique, MRI can also be used to determine the structure of chemical compounds

Metal hydride:

A hydride bound to a metal atom

Metalloprotein:

A protein that contains a metal ion cofactor

N:

Nitrogen, a gaseous element

N2 :

Dinitrogen, a chemically inert molecule formed by a strong triple covalent bond between two nitrogen atoms

N2O:

Nitrous oxide, a significant greenhouse gas

Nc :

Homocitrate complex; a ring structure comprising part of the iron-molybdenum cofactor of nitrogenase where N2 is bound and reduced to ammonia (nitrogen fixation)

NH2 :

An amido functional group

NH3 :

Ammonia; a chemically reactive nitrogen source that can be taken up and used by plants and serves as a significant source of plant nutrition

Ni:

Nickel, a metal element

Ni2+ :

Nickel ion resulting from the removal of electrons

Neutron:

A subatomic particle with no net electrical charge and a mass slightly larger than that of a proton

Nitrification:

The biological oxidation of ammonia with oxygen to nitrite (NO2 −) and with further oxidation to nitrate (NO3 −). A significant step in the nitrogen cycle in soil, it is performed by two groups of microorganisms: (a) ammonia-oxidizing bacteria such as Nitrosomonas and Nitrosococcus species and (b) ammonia-oxidizing archaea such as Crenarchaeota. The oxidation of nitrite to nitrate (the second step in the reaction) is mostly carried out by Nitrobacter species

O2 :

Oxygen molecule formed by the double covalent bond between two oxygen atoms

OLCN :

Oxygen limitation coefficient of nitrogenase; calculated as the ratio of total nitrogenase activity (TNA) to potential nitrogenase activity (PNA) in an atmosphere of 20% O2. It is used to estimate the limitation of O2 on nitrogenase activity in legume root nodules

Oxidation state:

A measure of the degree of oxidation of an atom in a substance

Oxidative phosphorylation:

A metabolic pathway that uses energy released by nutrient oxidation to generate ATP, which is used to drive cell metabolism

Pi :

Inorganic phosphate

Partial pressure:

In a mix of ideal gases, each gas possesses a partial pressure equal to the pressure the gas would exert if it alone occupied the volume at the same temperature as the gas mixture. The total pressure of a gas mixture then is the sum of all the partial pressures of each gas in the mixture

pD2 :

Partial pressure of deuterium

pH2 :

Partial pressure of hydrogen

pN2 :

Partial pressure of dinitrogen

pO2 :

Partial pressure of oxygen

P-cluster:

A cluster of eight iron atoms and seven sulphur atoms that routes electrons from the iron protein to the iron-molybdenum cofactor of the nitrogenase enzyme

Periplasmic space:

The space between the inner cytoplasmic membrane and the outer membrane of Gram-negative bacteria such as rhizobia or the equivalent space between the cell membrane and cell wall in Gram-positive bacteria (it is much larger in Gram-negative bacteria)

PGPR:

Plant growth–promoting rhizobacteria; bacteria that live within, on or nearby plant roots and exert effects beneficial to plant growth

Plasmid:

Extrachromosomal DNA separate from chromosomal DNA and capable of autonomous replication. It is often circular and double-stranded and is mostly found in bacteria; a bacterium may carry one to thousands of copies of a particular plasmid and these often harbour antibiotic resistance genes or toxin-producing genes. In rhizobia, plasmids often carry genes for nodulation, nitrogen fixation and HUP (sym plasmids)

Plasmodesmata:

Microscopic pores in plant cell walls that allow transport through the symplastic pathway

PNA:

Potential nitrogenase activity; the peak total nitrogenase activity obtained during a given increase in pO2. The PNA represents the nitrogenase activity that can be reached under O2-saturated conditions

ppm:

Parts per million

RNA:

Ribonucleic acid; similar to DNA but is comprised of ribose as opposed to deoxyribose (missing an oxygen atom) and uses uracil as a base to pair with adenine as opposed to thymine as in DNA; it is also generally single-stranded, whereas most DNA is double-stranded. RNA is the carrier of genetic information in viruses and is essential to protein synthesis in multicellular organisms

Radical:

In chemistry, an atom, molecule or ion likely to participate in chemical reactions

RE:

Relative efficiency; this is the proportion of total nitrogenase activity (TNA) that goes towards actual nitrogen fixation instead of H2 production. It is calculated as equalling 1 − (H2 evolved in air)/(acetylene reduced)

Reduction–oxidation (redox) reactions:

Changes in oxidation states of molecules or atoms via biochemical reactions. Reduction equals the gain of electrons/hydrogen or loss of oxygen leading to a decrease in oxidation state, whereas oxidation is the loss of electrons/hydrogen or gain of oxygen leading to an increase in oxidation state, but not all redox reactions involve transfer of electrons

Ribosomal DNA (rDNA):

Sequences encoding ribosomal RNA that regulates amplification and transcription. These sequences are useful in taxonomy because they are both highly conserved and yet variable enough to distinguish between groups or species

Rhizobacteria:

Bacteria that colonize the rhizosphere and/or the exterior or interior of plant roots

Rhizosphere:

The narrow region of soil directly influenced by root secretions and associated soil microorganisms

RQ:

Respiratory quotient; the ratio of CO2 evolved to O2 consumed

S:

Sulphur, a non-metallic element

Sink:

Where something is imported into, for example, soil is a hydrogen sink because H2 is imported into the soil from legume root nodules and stays there to be consumed by H2-oxidizing bacteria

Source:

Where something originates and is exported from, for instance, soil was originally thought to be a hydrogen source because it was believed that H2 from root nodules escaped from the soil into the atmosphere

STP:

Standard temperature and pressure; according to the International Union of Pure and Applied Chemistry (IUPAC), STP is equal to a temperature of 0°C (32°F or 273.15 K) and the absolute pressure of 100 kPa (14.504 lb per square inch or 0.986 atmospheres). The absolute pressure is zero referenced against a perfect vacuum representing a gaseous pressure of exactly zero

Symbiosis:

A close, frequently long-lasting relationship between two differing biological species. These relationships can be mutualistic, where both partners benefit; commensal, where one partner benefits and the other is unaffected, or parasitic, where one partner benefits and the other is harmed. A symbiont is a partner in a symbiotic relationship; the rhizobia-legume symbiosis is an example of a mutualistic relationship, where the rhizobia fix nitrogen for the plant and the plant provides nourishment and a safe environment for the bacteria

Symplast:

The inner side of the plasma membrane in plant cells in which H2O and small molecules can diffuse freely but larger molecules must be actively transported

Symplastic pathway:

Through the cytoplasm of plant cells

TNA:

Total nitrogenase activity; the total flow of electrons through the nitrogenase enzyme

Transposon/minitransposon:

A sequence of DNA that can move around to different positions within the genome of a single cell (transposition); it is also known as a mobile genetic element or ‘jumping gene’. This can cause mutations and vary the amount of genomic DNA within a cell. A minitransposon is the generic name for genetic material derived from transposons Tn10 and Tn5 in which naturally occurring functional DNA segments have been artificially rearranged to give shorter mobile elements

Urea:

(NH2)2CO; an organic compound significant in the metabolism of nitrogenous compounds of animals and the main nitrogenous substance present in the urine of mammals

Ureide:

Any of several compounds derived from urea by the replacement of one or more hydrogen atoms by an acid radical

V:

Vanadium, a rare metallic element

Vmax:

The maximal velocity of an enzyme when saturated with substrate

X-ray crystallography:

A technique to determine atomic arrangement in a crystal. An X-ray beam strikes a crystal and diffracts into multiple directions; the intensities and angles of the diffracted beams produce a three-dimensional image of the crystal’s electron density. From this, the approximate positions of atoms in the crystal can be determined. This method was used to elucidate the structure of DNA

Xylem sap:

In higher plants, the xylem is the vascular tissue used to transport water and nutrients; the xylem sap is the substance in xylem comprised mostly of H2O and inorganic ions but can also contain several organic compounds, such as hormones

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  1. Department of Biology, Saint Mary’s University, 923 Robie Street, Halifax, NS, B3H 3C3, Canada

    Zhongmin Dong

  2. Department of Biology, Dalhousie University, 1355 Oxford Street, Halifax, NS, B3H 4J1, Canada

    Amber-Leigh Golding

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Golding, AL., Dong, Z. Hydrogen production by nitrogenase as a potential crop rotation benefit. Environ Chem Lett 8, 101–121 (2010). https://doi.org/10.1007/s10311-010-0278-y

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