Phylogenetic analysis enabled us to compare the nifH gene sequences obtained from the Schizothrix mat with those available in the public database representative of the orders Nostocales and Oscillatoriales. As most of the nitrogenase sequences published in the database belonged to uncultivated microorganisms that have not been identified, we also included sequences from the environmental samples and strains previously isolated from cyanobacterial communities in the Muga River Fig.
This phylogenetic analysis highlights the clear separation of non-heterocystous and heterocystous cyanobacteria, in which the majority of nifH gene sequences recovered from the S chizothrix mat clustered with the sequences from the order Oscillatoriales. Most of these clustered with the sequence of the isolated strain MU51 Fig.
The Nostocales-like nifH sequences from the Schizothrix mat and the previously isolated heterocystous strains were distributed on different branches mixed with sequences of the database belonging to order Nostocales.
Sequences obtained in this study are indicated in bold. The sequence from the isolated strain MU51 is indicated by a dot. Nucleotide sequences obtained from this study were compared with information available from the National Center for Biotechnology.
These sequences, our own ones, and that of an outgroup were used for the phylogenetic analysis. The scale bar represents 0. The three isolated strains had low growth rates when grown without gassing or stirring on a nitrate medium Fig. All three had a generation time of approximately 9 days. Only the MU51 strain was able to grow in a medium without combined N and maintained its characteristic green colour throughout the experiment. This result suggests that MU51 was able to fix atmospheric N 2 and grow with N 2 as the only source of nitrogen.
The other two strains did not grow on the medium without combined nitrogen. They exhibited a progressive decline in chlorophyll concentration until they were pale yellow in colour at the end of the experiment. Cells were grown for two weeks in a medium with nitrate green boxes or in a medium without combined nitrogen brown boxes. The raw data are shown as scatter plots.
The low growth rates of these strains made it difficult to obtain sufficient biomass to assess their ability to fix N 2 with the acetylene reduction assay. Therefore, to avoid a long incubation with acetylene, which can be toxic for the cells 20 , we used the most direct and accurate method of incorporation of 15 N 2. This was confirmed by their lack of growth in the absence of combined nitrogen. Nutrient loading, concentration and ratios are strong selective forces shaping cyanobacterial communities in running waters.
Similar to other mountain rivers, the Muga River showed a low level of combined N. However, the dominant community is a pink-pigmented cyanobacterial mat see Fig. This finding is consistent with that of Stal 1 , who reported that the vast majority of microbial mats are composed of non-heterocystous cyanobacteria. However, the Schizothrix mat in this river has a simple structure because it develops directly on the bed of rocks and lacks the deep layers of sediment characteristic of most microbial mats.
This simplicity is reflected in the 16S rRNA gene diversity, the analysis of which revealed only the presence of sequences belonging to filamentous non-heterocystous cyanobacteria Oscillatoriales. The sequences of our Schizothrix cultures as well as the majority of the other cloned sequences from this mat were included in the same cluster. Another Schizothrix sequence from the database, which was also included in the tree, is not closely related to the sequences obtained from the mat, most likely related to its occurrence in a different marine habitat Similar results have been found in freshwater benthic mat-forming cyanobacteria isolated from New Zealand 25 and other environments, including extreme polar environments and thermal springs 26 , 27 , whereby filamentous types of cyanobacteria from the order Oscillatoriales with thin trichomes were found to be the most abundant group.
It has been argued that the absence of heterocystous cyanobacteria from the microbial mats is due to their lack of gliding motility, which is mainly a characteristic of non-heterocystous cyanobacteria 1. This property is important for optimal vertical positioning and allows for the compensation of the rapidly shifting physicochemical gradients in microbial mats 1.
The fact that non-heterocystous cyanobacteria were dominant in a river with low levels of combined nitrogen is striking because to the best of our knowledge, no diazotrophic abilities have been described for non-heterocystous cyanobacteria from running waters. Given its potential for nitrogen fixation and similar values in nitrogenase activity to those found in nearby heterocystous Rivularia colonies, other specific traits may explain niche differentiation.
Many mat-forming Schizothrix populations grow in aquatic environments that are subject to alternating periods of great moisture or even being submerged with periods when they are almost or completely dry Schizothrix mats from the Muga River typically grow in shallow areas with only a thin film of water under low flow and are conspicuous on the dry riverbank.
The brick colour typical of the outer part of the mats exposed to full daylight 28 was observed in these parts of the river see Fig. Therefore, in addition to potential nitrogen fixation, specific ecological niche occupancy in a system with changing flows, such as the Muga River at this site 17 , may explain the dominance of Schizothrix mats in these running waters.
Cantonati et al. The results show that the Schizothrix mat fixes N 2 in the light at similar rates to those of a heterocystous cyanobacterium located nearby in the river. It should be noted that these rates are lower than those reported for other cyanobacterial mats, such as those from marine habitats However, rates of nitrogenase activity in running waters from mountain ecosystems or similar systems with low water temperatures are typically low The results of our N 2 fixation survey were similar to those obtained from subalpine oligotrophic streams in the Rocky Mountains of North America 33 , 34 and from Antarctic streams 35 , A few exceptions have shown that N 2 fixation rates in streams can be higher.
Grimm and Petrone 31 reported high rates in desert streams during summer and autumn. Variations in N 2 fixation rates have been explained in terms of the availability of inorganic N but also with respect to temperature and light 31 , 33 , 34 , Nonetheless, it should also be noted that N 2 fixation rarely exceeds nitrate or ammonium uptake Marcarelli and coworkers 7 compared N 2 fixation rates from a wide variety of streams, reporting that the median N fixation was 80— times lower than median DIN uptake fluxes.
This is a similar value to those that we have found. On the other hand, ambient stream water temperature directly affects N 2 fixation. Increased temperatures stimulate N 2 fixation in all streams analysed 31 , 32 , 33 , However, it is difficult to discern which factor exerts the strongest influence because these parameters tend to covary Further research is needed to quantify the incidence of such characteristics, which may help explain the spatial and temporal variation in N 2 fixation rates.
The finding that nitrogenase activity occurs in the light was unexpected because it has been widely reported that cyanobacterial mats that are dominated by non-heterocystous cyanobacteria usually only show substantial rates of nitrogenase activity in the dark 38 , These results raised the question about what kind of diazotrophs are responsible for the N 2 fixation in this mat.
The addition of DCMU to the Schizothrix mat produced a significant increase in nitrogenase activity, as usually occurs in non-heterocystous cyanobacteria 1 , 3 , 39 , whereas the addition of DCMU to heterocystous cyanobacteria caused a significant decrease in nitrogenase activity in the light 1 , 4 , The results of the laboratory experiments also indicated that at least one of the main strains of non-heterocystous cyanobacteria from the Schizothrix mat can fix N 2. This is also consistent with the results of the analysis of the nifH gene.
The majority of nifH sequences retrieved from the samples were related to Oscillatoriales-type nifH. Some of these sequences belonged to one of the dominant Schizothrix morphotypes isolated, which in turn was able to grow in the absence of combined nitrogen and to exhibit nitrogenase activity.
These results suggested that nitrogen fixation in these mats may be attributed to non-heterocystous cyanobacteria. However, it has been argued that different mechanisms such as nifH -degenerated primers, polyploidy in cyanobacteria and differential DNA extraction could bias nifH clone libraries against heterotrophic diazotrophs Therefore, the importance of these nitrogen-fixing organisms may have been underestimated in analyses of early successional biological soil crust communities Therefore, although our results indicate that the primary diazotrophs in the mats are cyanobacteria because all the recovered sequences belonged to this group, in spite of the use of general primers for aerobic and microaerophilic diazotrophs, we cannot discount the potential for fixation by non-phototrophic bacteria stimulated by cyanobacteria-released metabolites in the light The ability to fix nitrogen in the light requires the development of mechanisms for protecting the O 2 -labile nitrogenase Paerl and coworkers 43 , 44 emphasized the importance of the formation of anoxic microzones in microbial mats and other systems in which N 2 fixation could proceed in an uninhibited manner.
In our study, the results from oxygen microelectrodes indicate the existence of internal O 2 -reduced microzones where nitrogen fixation may be concentrated.
Stal et al. In addition, we propose that enhancement of oxygen-scavenging mechanisms, such as high respiration rates, may be supplementary ways of protecting nitrogenase activity, as has also been proposed for Trichodesmium The addition of DCMU had an alleviating effect due to the decreased O 2 production at the water-splitting site of PSII, thereby allowing nitrogenase activity to attain its maximal rate.
Under these conditions, ATP had to be supplied mainly by cyclic phosphorylation and the reductant supplied by aerobic respiration, which in turn decreased O 2 concentration. Under strictly anaerobic conditions in the light, nitrogenase also showed maximal rates of activity. Here, again, ATP had to be supplied by cyclic phosphorylation, whereas the reducing power could be derived from fermentative metabolism.
Dark aerobic conditions did not facilitate significant levels of nitrogenase activity in the Schizothrix mat unless exogenous fructose was supplied. The addition of fructose increased respiratory metabolism, thereby decreasing oxygen tension and increasing the supply of ATP and reductant to a level compatible with maximal rates of N 2 fixation. However, under anaerobic conditions, exogenous fructose failed to support nitrogenase activity, indicating that fermentative metabolism by itself cannot provide enough ATP and reductant for nitrogen fixation.
The Mehler reaction, which occurs in cyanobacteria via direct photoreduction of O 2 to water without the production of significant amounts of reactive oxygen species, as occurs in eukaryotes 47 , may also alleviate the negative effect of increasing O 2 production at PSII. In addition, increased Mehler activity could generate excess ATP through cyclic electron transport, which is needed to support nitrogen fixation 48 , 49 , In conclusion, although we cannot discount the possibility that non-phototrophs contribute to nitrogen fixation in the Schizothrix mat, all of our results the microscopic observations, the 16S rRNA and nifH gene analyses, the effect of DCMU on nitrogenase activity, and the physiological experiments on isolated strains are consistent with our hypothesis that non-heterocystous cyanobacteria are driving nitrogen fixation in the mats.
These diazotrophs may be important contributors to the nitrogen fixed in this river and merit further scrutiny. The field site and water sampling and analysis procedures have previously been described in detail Samples of the cyanobacterial communities were collected with the help of a knife blade because their structure does not allow the use of a metal core. The fresh weight of all the samples was determined with a field balance after gently placing the samples on filter paper to eliminate water droplets.
Samples for determinations and genetic analysis were frozen in liquid nitrogen before transportation. Fieldwork was carried out from 9 to 11 May The river flow during this time was moderate average of 0. Morphological observations of microbial mats were made under a dissecting microscope Leica, Leica Microsystems and an Olympus BH2-RFCA photomicroscope equipped with phase-contrast and epifluorescence.
All of the important key features that were taken into consideration to identify natural samples, such as cell width, cell length, attenuation of apical cells, and sheath morphology, were studied in samples of 25—50 cells. This procedure was repeated with the same sample until no more pigment could be extracted. The percentage abundance in natural samples was evaluated by counting the presence of each morphotype as cells in a filament or as equal numbers of individual cells.
To simulate the chemical conditions of the river water, cyanobacteria were isolated on Petri dishes with a 1. Three strains were successfully isolated from the Schizothrix mats from the Muga River, each from a single trichome. Photosynthetic activity was measured using the stable isotope technique 13 C uptake as previously described The DIC content of the water was calculated from its alkalinity, determined by acid titration, taking the pH and temperature into consideration.
Two profiles of photosynthetic activity were derived at different positions on each of the three replicates of each mat. The uptake of N from ammonium and nitrate was measured using the stable isotope technique as previously described Nitrogenase activity of the Schizothrix mats was measured using the acetylene reduction technique as previously described 4.
Control bottles containing river water without mat samples were also incubated to check for other possible sources of ethylene aside from the cyanobacterial communities. The plastic bottles were capped with reversible rubber stoppers and covered with parafilm to ensure gas-tightness.
The samples were secured to the streambed as described above. Special care was taken to ensure that the samples were positioned with the surface layer facing upwards and to avoid overlapping.
These tubes give a peak at the same retention time as a concentration of ethylene equivalent to 0. The detection limit of the chromatographic method was 0. To improve the reliability of the data, any values below 0. To eliminate any errors arising from contaminants, ethylene production was quantified as the difference between the final and initial samples.
A mat sample was considered to exhibit nitrogenase activity if differences in ethylene concentration between the initial and final gas samples were significant paired t-test. In the laboratory experiments, samples of the Schizothrix mat were incubated in triplicate in ml Erlenmeyer flasks approximately 0.
Nitrogen fixation of the isolated strains was measured using the stable isotope 15 N 2. A gas-tight syringe was used to inject 0. Finally, a 0. After incubation, samples were rinsed three times with culture medium without nitrogen to eliminate any unincorporated 15 N. Additional samples of each culture were taken before the start of the experiment to determine the natural abundance of 15 N. DNA was extracted as previously described 11 , Recombinant clones carrying the correct size insert were purified and sequenced as previously described The nifH sequences were translated and the amino acid sequences were aligned.
Trees were constructed using neighbour-joining NJ algorithms Bootstrap analysis of replicates was performed for each consensus tree ANOVA with Tukey post hoc testing, independent sample t-tests, and paired sample t-tests were used to compare group differences. The SigmaStat program V2. How to cite this article : Berrendero, E. Nitrogen fixation in a non-heterocystous cyanobacterial mat from a mountain river. Stal, L.
Whitton, B. Chapter Google Scholar. Paerl, H. Cyanobacterial-bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environ Microbiol 2 , 11—15, doi: Bebout, B. Identification of the sources of energy for nitrogen fixation and physiological characterization of nitrogen-fixing members of a marine microbial mat community. Microb Ecol 42 , —, doi: Article PubMed Google Scholar.
Severin, I. Light dependency of nitrogen fixation in a coastal cyanobacterial mat. ISME J 2 , —, doi: Livingstone, D. Diel variations in nitrogen and carbon-dioxide fixation by the blue-green alga Rivularia in an upland stream. Marcarelli, A. Is in-stream N2 fixation an important source for benthic communities and stream ecosystems? J N Am Benthol Soc 27 , —, doi: Article Google Scholar. Scott, J. The plant cyanobionts are members of the genus Nostoc , which is commonly found free-living in nature Dodds et al.
However, in the laboratory, other hormogonium-developing cyanobacterial genera, such as Calothrix and Chlorogloeopsis , may infect liverworts West and Adams, Members of the genus Nostoc are primarily non-motile, but a characteristic of the genus is the ability to produce specialized motile filaments known as hormogonia which serve as a means of dispersal as well as plant infection Meeks and Elhai, Hormogonia development is triggered by a variety of environmental factors, including plant-derived chemical signals.
The development of hormogonia in heterocystous cyanobacteria results from a round of rapid, synchronous cell divisions which result in a decrease in cell size Meeks and Elhai, This is followed by fragmentation of the filament at the heterocyst—vegetative cell junctions, releasing short, motile hormogonia.
Hormogonia lack heterocysts and are a temporary stage in the Nostoc life-cycle, soon returning to vegetative growth and developing heterocysts once more. For hormogonia to locate the symbiotic tissue of a plant host they must attach to the surface and both extracellular polysaccharides and pili fimbriae are thought to play a role in this process Adams, Type IV pili are required for gliding in some unicellular cyanobacteria Bhaya, , and the cell surface of hormogonia of the symbiotically competent Nostoc punctiforme is covered with pili Duggan et al.
Plant hosts increase the likelihood of infection by cyanobacteria by both stimulating the formation of hormogonia in potential cyanobionts and by guiding the hormogonia to the symbiotic tissues by chemotaxis. Hormogonia formation is stimulated by hormogonia-inducing factors HIFs. HIF production has been found in the hornwort Anthoceros punctatus Meeks, , as well as cycads and the angiosperm Gunnera Rasmussen et al.
Anthoceros punctatus HIF is a small, heat-labile product released by the hornwort when starved of combined nitrogen Meeks and Elhai, ; Meeks, Nostoc punctiforme mutants with increased sensitivity to Anthoceros HIF, also show a greater initial frequency of infection of the hornwort than the wild type Cohen and Meeks, The partners in the Azolla symbiosis.
A Fronds of the Azolla filiculoides Lam. C , D , E Light micrograph of the cyanobiont. Pairs of megasporocarps blue develop at the underside of the cyanobacterial colonized Azolla leaves. Filaments of the motile cyanobacterial cell stage red , the hormogonia h , are attracted to the sporocarps, gather at the base and subsequently move towards the tip, before entering the sporocarps via channels white arrows.
Once inside the sporocarp the hormogonia differentiate into individual thick walled resting spores or akinetes; ak , seen as the intensively red fluorescing small inoculum on top of the megaspores sp. Ran et al. The infection of hornworts via the stomata-like opening to the slime cavity has interesting parallels with the likely method of entry of cyanobacteria into the primitive, extinct land plant Aglaophyton major.
This symbiosis is only known from fossil evidence, but an Archaeothrix -type filamentous cyanobacterium is thought to have entered the plant via stomatal pores Taylor and Krings, The cyanobacteria are thought to have initially colonized the substomatal chambers and then spread throughout the outer cortical tissue, where they can be seen in fossil specimens of the plant.
Once the cyanobacterium has entered the host plant a number of morphological, developmental, and physiological changes occur. The development of hormogonia is repressed, whereas the development of heterocysts is greatly stimulated. The rate of cell division is reduced, ensuring that the cyanobiont does not outgrow the host. The rate of CO 2 fixation is greatly reduced, whereas nitrogen fixation is stimulated and ammonium assimilation down-regulated Figure 5.
The nitrogen fixation rates for cyanobacteria symbiotically associated with bryophytes are several-fold higher than for the same free-living cyanobacteria. The level of GS protein in Anthoceros -associated Noctoc is similar to that in free-living cyanobacteria, but GS activity is reduced implying that activity is regulated by an unknown, and presumably plant-regulated, post-translational modification of the enzyme.
Close examination of an Azolla leaf reveals that it consists of a thick, greenish or reddish dorsal upper lobe and a thinner, translucent ventral lower lobe emersed in the water. It is the upper lobe that has an ovoid central cavity, the "living quarters" for filaments of Anabaena. Probably the easiest way to observe Anabaena is to remove a dorsal leaf lobe and place it on a clean slide glass with a drop of water.
Then apply a cover slip with sufficient pressure to mash the leaf fragment. Under X magnification the filaments of Anabaena with larger, oval heterocysts should be visible around the crushed fern leaf. The thick-walled heterocysts often appear more transparent and have distinctive "polar nodules'' at each end of the cell.
The "polar nodules" may be the same composition as cyanophycin granules co-polymer of arginine and aspartic acid. Cyanophycin granules occur in many cyanobacteria and may serve as a nitrogen storage product. Although Azolla can absorb nitrates from the water, it can also absorb ammonia secreted by Anabaena within the leaf cavities. Rice is the single most important source of food for people and Azolla plays a very important role in rice production. For centuries Azolla and its nitrogen-fixing partner, Anabaena, have been used as "green manure" in China and other Asian countries to fertilize rice paddies and increase production.
Republic of China has 3. Extensive propagation research is being conducted in China to produce new varieties of Azolla that will flourish under different climatic and seasonal conditions.
According to some reports, Azolla can increase rice yields as much as percent per year. Rice can be grown year after year, several crops a year, with little or no decline in productivity; hence no rotation of crops is necessary. In addition to nitrogen fixation, Azolla has a number of other uses. Several California aquafarms grow Azolla in large vats of circulating fresh water. Apparently fish and shrimp relish the Azolla. In fact, Azolla was grown for fish food and water purification at the Biospere II project in Arizona a 2.
Fresh Azolla and duckweed Wolffia can also be used in salads and sandwiches, just as alfalfa and bean sprouts are used. Dried, powdered Wolffia and Azolla make a nutritious, high protein powder similar to the popular alga cyanobacterium Spirulina that is sold in natural food stores.
Azolla has also proved useful in the biological control of mosquitos. The mosquito larvae are unable to come up for air because of the dense layer of Azolla on the water surface. Azolla grows very quickly in ponds and buckets, and in makes an excellent fertilizer green manure and garden mulch. Schematic illustration of important metabolic and geneticin formation pathways in NoAz.
The nitrogen cycle of Earth is one of the most critical yet poorly understood biogeochemical cycles. Of this, a single non-heterocystous genus, Trichodesmium sp.
Geochemical evidence suggests that, on a global scale, nitrogen fixation does not always keep pace with denitrification on time scales of centuries to millenia Falkowski and Raven, , yet it remains unclear what process es limits nitrogen fixation in the oceans. More importantly, given the potential for heterocystous cyanobacteria to outcompete organisms such as Trichodesmium , it is unclear why the apparent tempo of evolution of marine diazotrophic cyanobacteria is so slow.
Finally, some Questions needs answering, Are there N 2 -fixing picoplankton? What limits the growth of N 2 -fixing microorganisms in the open ocean? Is N 2 fixation associated with zooplankton? Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution 3.
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Downloaded: Introduction Cyanobacteria are often called "blue-green algae", this name is convenient for talking about organisms in water that make their own food, but does not reflect any relationship between the cyanobacteria and other organisms called algae.
Cyanobacteria that can fix N 2 aerobically A1. Cyanobacteria that separate N 2 fixation from oxygenic photosynthesis in space. Includes heterocystous genera, for example, Anabaena. Cyanobacteria that separate N 2 fixation from oxygenic photosynthesis in time.
Includes non-heterocystous genera, such as Gloeothece , Cyanothece and Lyngbya A3. Cyanobacteria that separate N 2 fixation from oxygenic photosynthesis both in space and in time. Includes non-heterocystous genera, such as Trichodesmium and Katagnymene B.
Cyanobacteria that can fix only N 2 either anaerobically or microaerobically Many non-heterocystous cyanobacteria,forexample, Plectonemaboryanum. Table 1. A classification of N 2 -fixing Cyanobacteria based on behavior. Unicellular group Unicellular strains growing on BG II medium without nitrogen Aphanothece,Gloeothece, Anabaena group: Heterocystous strains with a thin sheath, without branching, do not form mucilaginous colonies of definite shape Anabaena,Nodularia, Cylindrosperinurn, Anabaenopsis etc.
Nostoc group: Heterocystous strains with a thick sheath, without branching, forming mucilaginous colonies of definite shape Nostoc Aulosira group: Heterocystous strains with a thick sheath, usually without branching, do not form diffuse colonies on agar medium Aulosira Scytoneina group: Heterocystous strains with false branching, without polarity, forming velvet-like patches on agar medium Scytonema Calothrix group: Heterocystous strains with false branching, with polarity, forming velvet-like patches on agar medium Calothrix, Tolypotkrix, Hassalia Gloeofrichia group: Heterocystous strains, with polarity, forming mucilaginous colonies of definite shape Gloeotrichia, Rivularia Fischerella group: Heterocystous strains with true branching Fischerella, Westiellopsis, Stigonerna.
Table 2. Name of the species Nitrogenase activity nmol C 2 H 4 mg dry wt. Strain CA 0. Strain N9AR 0. Table 3. Nitrogenase activity of various cyanobacterial species.
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More statistics for editors and authors Login to your personal dashboard for more detailed statistics on your publications. Access personal reporting. More About Us. Cyanobacteria that can fix N 2 aerobically. Includes non-heterocystous genera, such as Gloeothece , Cyanothece and Lyngbya. Includes non-heterocystous genera, such as Trichodesmium and Katagnymene. Cyanobacteria that can fix only N 2 either anaerobically or microaerobically.
Many non-heterocystous cyanobacteria,forexample, Plectonemaboryanum. Anabaena group:. Heterocystous strains with a thin sheath, without branching, do not form mucilaginous colonies of definite shape Anabaena,Nodularia, Cylindrosperinurn, Anabaenopsis etc.
Heterocystous strains with a thick sheath, without branching, forming mucilaginous colonies of definite shape Nostoc. Aulosira group:. Heterocystous strains with a thick sheath, usually without branching, do not form diffuse colonies on agar medium Aulosira.
Scytoneina group:. Heterocystous strains with false branching, without polarity, forming velvet-like patches on agar medium Scytonema. Calothrix group:. Heterocystous strains with false branching, with polarity, forming velvet-like patches on agar medium Calothrix, Tolypotkrix, Hassalia. Gloeofrichia group:. Heterocystous strains, with polarity, forming mucilaginous colonies of definite shape Gloeotrichia, Rivularia.
Journal of Bacteriology , Diaz, R. Spreading dead zones and consequences for marine ecosystems. Science , Fattah, Q. Bangladesh Botanical Society, Dhaka, Bangladesh, Kamst, E. Plant-Microbe Interactions , eds. Plenum Publishing, New York, Herridge, D. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil , Hubbell, D. Biological Nitrogen Fixation.
Napoli, C. Ultrastructure of Rhizobium-induced infection threads in clover root hairs. Applied and Environmental Microbiology 30 , National Research Council. Biological Nitrogen Fixation: Research Challenges. Postgate, J. The Fundamentals of Nitrogen Fixation. Stephan, M. Volume I, eds.
Vance, C. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resouces. Plant Physiology , Van Rhyn, P.
The Rhizobium-plant symbiosis. Microbiological Reviews 59 , Vadakattu, G. Free-living bacteria lift soil nitrogen supply. Farming Ahead , 40 Vitousek, P.
Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7 , CO;2 Vlassak, K. Introduction to the Basic Drivers of Climate.
Terrestrial Biomes. Coral Reefs. Energy Economics in Ecosystems. Biodiversity and Ecosystem Stability. Ecosystems Ecology Introduction. Factors Affecting Global Climate. Rivers and Streams: Life in Flowing Water. The Conservation of Mass. The Ecology of Carrion Decomposition.
Causes and Consequences of Biodiversity Declines. Earth's Ferrous Wheel. Alternative Stable States. Recharge Variability in Semi-Arid Climates. Secondary Production. Food Web: Concept and Applications.
Terrestrial Primary Production: Fuel for Life. Citation: Wagner, S. Nature Education Knowledge 3 10 Aa Aa Aa. Figure 1. Nitrogen-fixing organisms found in agricultural and natural systems.
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