BIOGEOCHEMISTRY OF NITROGEN
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- Ami Ryan
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1 BIOGEOCHEMISTRY OF NITROGEN I. Introduction II. N-cycle and the Biochemistry of N III. Global N Patterns/Budget (Galloway et al. 1995) IV. Patterns of N at the HBEF V. Inputs, Effects and Management of Anthropogenic N in the Northeast
2 I. INTRODUCTION Nitrogen is a difficult element to study. Nitrogen has many different chemical species, phases and oxidation states. -III NH 4 + NH 3 Org N (g, aq, s) 0 N 2 (g) Reduced (molecular N) +I N 2 O (nitrous oxide) (g) +II NO (nitric oxide) (g) +III NO 2 - (nitrite) (aq) Oxidized +IV NO 2 (nitrogen dioxide) (g) +V NO 3 - (nitrate) Nitrogen is an interesting element because some pools (N 2, Org N) are large and generally unavailable. N is an important element because: 1. It is a macronutrient (protein); 2. At elevated concentrations, it may cause adverse environmental effects (NH 3, NH 4+, NO 2-, NO 3- ). (aq)
3 N Utilization II. N-CYCLE, AND THE BIOCHEMISTRY OF N 1. Assimilatory - used for biosynthetic reactions (amino acid production), not directly used in energy metabolism - All living organisms require N. 2. Dissimilatory processes - Nitrogen is taken up in a particular form (oxidized or reduced), for specialized reactions involving ATP production and excretion of a N product. Dissimilatory N is not incorporated into the physical or biochemical structure of an organism - Only a few specialized organisms can utilize dissimilatory processes. N Assimilation Nitrogen in biomass largely occurs as the reduced oxidation state (-III), so this is the energetically favored form of N. However, NO 3- is generally preferred by plants. This may be due to greater mobility of NO 3-. Energy must be expended by plants or microbes to extract NH 4+ from soil and sediments. Also, competition of NH 4+ with other cations on enzymes. Plants/microorganisms can commonly assimilate NH 4+, NO 3- in water or soil. The role of organic N as a nutrient source is not well established. Some coniferous trees have been shown to assimilate dissolved organic N.
4 N-cycle, and the Biochemistry of N (cont.) If N is taken in as NH 4+, it is directly used by organisms in biosynthesis. If N is assimilated as NO 3-, it must be reduced within the cell. Two enzymes are involved: 1. Nitrate reductase - contains molybdenum NO 3- + NADH + H + = NO 2- + H 2 O + NAD + 2. Nitrite reductase NO NADH + 5H + = NH H 2 O + 3NAD + Some organisms have the unique characteristic to assimilate molecular N - nitrogen fixation. This process requires the enzyme, nitrogenase, which is a complex protein containing iron, molybdenum and inorganic S as part of its structure. The process is extremely energy-intensive, as you might expect, to break a triple bond. N N
5 N-cycle, and the Biochemistry of N (cont.) Only a few species of microorganisms can fix nitrogen. These include free-living organisms (asymbotic, e.g. Clostridium, Azobacter, Azospirillum, and Anabena) and organisms in symbiotic relationships with roots (e.g. Rhizobium, Frankia). N H + + 8e - + natp + nh 2 O = 2NH 4+ + H 2 + nadp + nh 2 PO 4 - where: n = (exact number uncertain) Ammonium assimilation occurs by two enzymatic routes: 1. Glutamine synthase COO - CONH 2 CH 2 CH 2 CH 2 + NH 4+ +ATP = CH 2 + ADP + H 2 O CHNH 3 + CHNH 3 + COO - COO - glutamate glutamine
6 N-cycle, and the Biochemistry of N (cont.) 2. Glutamate dehydrogenase COO - COO - CH 2 CH 2 CH 2 + NADH + H + + NH + 4 = CH 2 + NAD + H 2 O C = O CHNH + 3 COO - COO - α-ketoglutarate glutamate
7 N-cycle, and the Biochemistry of N (cont.) In addition, Glutamate synthase is used in plants and microorganisms to convert amido-nitrogen of glutamine back to glutamate for amino acid systems. Glutamate synthase COO - CONH 2 COO - CH 2 CH 2 CH 2 CH 2 + NADH + H + + CH 2 = 2 CH 2 + NAD + C = O CHNH 3 + CHNH 3 + COO - COO - COO - α-ketoglutarate glutamine glutamate
8 N-cycle, and the Biochemistry of N (cont.) Mineralization Mineralization is the decomposition of organic matter to inorganic matter. This is accomplished by heterotrophic microbes. The release of N is generally thought to be a by-product of the use of soil organic C as an energy source. R - NH 2 = NH 3 + H 2 O = NH 4+ + OH - Mineralization of organic matter is critical to the supply of nutrients to vegetation in terrestrial environments (see Table). Mineralization is directly related to the nitrogen content of soil and the availability of organic carbon. Vegetation with higher C:N in litter generally shows lower rates of mineralization in soil. Urea NH 2 urease C = O + 2H 2 O + 2H + = 2NH 4+ + H 2 CO 3 NH 2
9 Percentage of the annual requirement of nutrients for growth in the Northern Hardwoods Forest at Hubbard Brook, New Hampshire, that could be supplied by various sources of available nutrients* Process N P K Ca Mg Growth requirement (kg ha -1 yr -1 ) Percentage of the requirement that could by supplied by: Intersystem inputs Atmospheric Rock weathering Intrasystem transfers Reabsorption Detritus turnover (includes return in throughfall and stemflow) *Reabsorption data are from Ryan and Bormann (1982). Data for N, K, Ca, and Mg are from Likens and Bormann (1995) and for P from Yanai (1992).
10 N-cycle, and the Biochemistry of N (cont.) Nitrogen Dissimilation Nitrification - the oxidation of NH 4 + NH O 2 = NO 3- + H 2 O + 2H + Two different species of lithotrophic organisms are responsible for this reaction. Nitrosomonas ammonia oxidase NH /2 O 2 = NO H + + H 2 O This oxidation/reduction sequence is not direct but includes an electron transport chain in which 1 mol of ATP is produced per mol of NH 4+ oxidized. This sequence is continued by the organism. Nitrobacter nitrite oxidase NO 2- + ½O 2 = NO - 3 The electron produced from the oxidation of NO 2- is also coupled with an electron transport cycle producing 1 mol of ATP.
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12 N-cycle, and the Biochemistry of N (cont.) Nitrification can also be accomplished by heterotrophic bacteria (Arthrobacter) and fungi (Aspergillus) which obtain no energy in this process. Importance is not clear but believed to be less than autotrophic nitrification) Nitrification is an important process because many factors influence it and because it converts nitrogen from a relatively immobile form (NH 4+ ) to a mobile form (NO 3- ). Because the organisms which mediate nitrification reactions are specific populations, they are easily disrupted. 1. Lithotrophic organisms use inorganic C (CO 2 ) to produce organic C through the Calvin cycle. This process is very energy intensive so these organisms have slow growth rates. 2. Nitrifiers, require well-oxygenated conditions. 3. Very sensitive to toxicants, trace metals. 4. Sensitive to ph (< 6?). N 2 O and NO are released via nitrification.
13 N-cycle, and the Biochemistry of N (cont.) Denitrification Denitrification is the process by which N is used as the terminal electron acceptor in a reduction reaction. This may be conducted by species: Pseudomonas, Bacillus, Vibrio and Thiobacillus. Because organisms favor O 2 reduction due to energetics, denitrification only proceeds under anaerobic conditions. Organisms produce 2 mol ATP per mol NO 3- reduced. The process proceeds through an electron transport chain. The reductant is generally organic matter, generally sugars or simple compounds (methanol used in waste water treatment). Reduced sulfur compounds can also be used (sulfur, sulfide). These electrons are transferred to the electron transport chain where the reduction occurs. In this process, NO 3- is first reduced to NO 2-. NO 3- + NADH + H + Through this process, ATP is produced. = NO 2- + NAD + + H 2 O
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15 N-cycle, and the Biochemistry of N (cont.) Subsequent reactions may occur: NO H + + e - = NO + H 2 O NO H + + 2e - = ½N 2 O + 3/2 H 2 O NO H + + 3e - = ½N 2 + 2H 2 O NO + 2H + + 2e - = ½N 2 + H 2 O ½N 2 O + H + + e - = ½N 2 + ½H 2 O The overall reaction to N 2 is C 6 H 12 O /5 NO /5 H + = 6CO /5 N /5 H 2 O The "leaky pipe" hypothesis suggests that trace gases, N 2 O and NO, are by-products of nitrification and denitrification.
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18 N-cycle, and the Biochemistry of N (cont.) Mechanisms of N Immobilization 1. Plant assimilation 2. Microbial (thought to predominate) bacteria fungal Critical C:N C 5 H 7 O 2 N higher C:N Above, microbial growth is N limited Little N leaching Below, microbial growth is C limited N leaching occurs 3. Nitrification, distribution of NH 4+, NO 3 - Abiotic immobilization Cation exchange X - -Na + + NH 4+ = X - -NH 4+ + Na + No significant mechanism for abiotic immobilization of NO 3- (anion exchange weak), but recent investigations have suggested the importance of abiotic N retention (Ferrous wheel hypothesis).
19 N-cycle, and the Biochemistry of N (cont.) N-Volatilization NH 4+ participates in an acid-base reaction. NH 4+ = NH 3 + H + ; pk a = 9.1 NH 3 also has the ability to volatilize. NH 3 aq = NH 3 g As a result, NH 3 can volatilize, but the reaction is only quantitatively important under high ph conditions. Forest soils are generally acidic, so NH 3 volatilization is an insignificant process. In agricultural lands, application of fertilizer (manure) can result in high ph conditions and significant NH 3 volatilization.
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23 N-cycle, and the Biochemistry of N (cont.) Stable Isotopes of N Stable isotopes of N can provide insight into biogeochemistry. 1. Addition tracer experiments 2. Natural abundance observations There are two stable isotopes of N: air composition 15 N = N = N/ 14 N = 1/272 Nitrogen isotopes are reported in values of per mil relative to atmospheric air. Delta notation δ 15 N = 15 N N sample N N std 15 N N std x1000
24 N-cycle, and the Biochemistry of N (cont.) Let's consider an example: sample 15 N = std 15 N = δ 15 N sample = x = 2.7 % 0 Note that this example suggests that the sample is slightly enriched in 15 N relative to the standard (+ sign). A negative value would indicate that the sample is depleted relative to the standard. In most terrestrial ecosystems, δ 15 N values range from -10 to +15. In absolute abundance, this represents a range of to atom % 15 N. Rule of thumb Organisms prefer the light isotope ( 14 N) over the heavy isotope ( 15 N) in transformations (see figures).
25 N-cycle, and the Biochemistry of N (cont.) The δ 15 N of a cumulative product is always lighter than the residual reactant. Consider denitrification. Say that this process fractionates by 5, 10, 20 from an initial NO 3- of 0. The first bit of product (N 2 ) is lighter than the reactant by the fractionation factor. As the reaction proceeds to completion, the product becomes progressively heavier until, at the end, it reaches its initial composition. The reactant also becomes progressively heavier until it is used up. Several factors influence the degree of fractionation: 1. Specific process. 2. Size of the pool. Large pools exhibit large fractionation, small pools exhibit little fractionation. 3. Temperature.
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27 N-cycle, and the Biochemistry of N (cont.) N Fractionation Process Qualitative Charge Literature N fixation small -3 to +1 Assimilation microbial small -1.6 to +1 (-0.52) plant small -2.2 to +0.5 (-0.25) Mineralization small -1 to +1 Nitrification large -12 to -29 Volatilization large > 20 Sorption/desorption small 1 to 8 Denitrification large -40 to 5
28 N-cycle, and the Biochemistry of N (cont.) Observations in the Literature Terrestrial Ecosystem Compartments 1. Plants are slightly depleted. 2. Organic soils are enriched. 3. Mineral soils are more enriched. The 15 N of plants is similar to what they assimilate (little fractionation). Variations in plant δ 15 N are due to: 1. rooting depth; deeper roots more enriched 2. NO 3- vs. NH 4+ preference; NH 4 + more enriched Rates of N Cycling In general, δ 15 N increases in ecosystems with increased rates of N cycling due to fractionation associated with nitrification and NO 3- loss. This is sometimes quantified as an enrichment factor (δ 15 N leaf - δ 15 N soil). See observations from Walker Branch, TN and Hubbard Brook.
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32 enrichment factor = δ 15 N leaf - δ 15 N soil.
33 Pardo et al. (2002) Natural abundance of forest floor at W6 at the HBEF
34 N-cycle, and the Biochemistry of N (cont.) Food Web Studies Food web studies show an enrichment in 15 N. N isotope scientists like to say you are what you eat, plus 3. See figure.
35 16 Carbon and Nitrogen Stable Isotopes in Oneida Lake Food Web from Mitchell et al. (1996) δ 15 N δ 13 C SEDIMENT SESTON DAPHNIA ZEBRA MUSSEL FLESH YELLOW PERCH SHAD WALLEYE
36 Adult Walleye Adult Yellow Perch Young-of-the-Year Fish (e.g., Yellow Perch and Gizzard Shad) Benthic Macroinvertebrates Pseudofeces Zooplankton (e.g., Daphnia) Zebra Mussels Benthic Algae Phytoplankton
37 N-cycle, and the Biochemistry of N (cont.) Use of 18 O and 15 N as a Tracer of Ecosystem N Retention There are some drawbacks to using 15 N as an ecosystem tracer due to its relatively narrow range. 18 O associated with NO 3- offers additional information as a tracer. Durke et al. (1994) used 15 N and 18 O together to evaluate the retention of atmospheric NO 3- to forests in Germany. See tables.
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39 N-cycle, and the Biochemistry of N (cont.) Table 1. Characteristics of sites studied. Atmospheric input 1 Springwater output Site No. Site Condition* NO 3 - (mmol m -2 yr -1 ) NH 4 + (mmol m -2 yr -1 ) NO 3 - concentration 2 (µmol 1-1 ) Total NO 3 - output 3 (mmol m -2 yr -1 ) 1 Healthy Declining, peaty soil Slightly declining Healthy Slightly declining, limed Slightly declining, limed Strongly declining Strongly declining SEE NEXT PAGE FOR FOOTNOTES
40 N-cycle, and the Biochemistry of N (cont.) Site conditions, atmospheric inputs of nitrogen to the watersheds, and NO 3- output characteristics of eight forest springs in the Fichtelgebirge (northeast Bavaria, Germany). *Definitions: slightly declining, single trees affected by needle yellowing and crown thinning; strongly declining, all trees affected. 1 Extrapolated from measurements of throughfall sampled between 15 April and 15 December 1992 with ten funnels per site. 2 Volume-weighted mean of monthly measurements in 1991 and Modelled from volume-weighted mean NO 3- concentration and seepage.
41 N-cycle, and the Biochemistry of N (cont.) Table 2. Nitrate in spring water Site No. Output on NO - 3 atm in spring water Fraction of total NO 3- output Absolute flux (%) (mmol m -2 yr -1 ) Fraction of NO 3- input (%) * *This value (>100% recovery) could have been caused by errors in the input-output balance, or by temporal NO 3 - atm storage in the aquifer.
42 ore recent work indicates that almost of the nitrate in soil and surface waters is microbially processed.
43 70 60 Delta 18 O ( o /oo) precipitation Soil + groundwater Delta 15 N ( o / oo ) General trends of 18-O and 15-N values of nitrate
44 Results of nitrate samples taken during snowmelt at Archer Creek Catchment, Huntington Forest (Piatek et al., 2005) Delta 18 O ( o / oo ) precipitation groundwater Delta 15 N ( o / oo )
45 III. GLOBAL N PATTERNS/BUDGET Across the Earth, N largely occurs as N 2 in the atmosphere (78%) and in the ocean and in soil. Nitrogen is divided into two broad classes: 1. Reactive - NO y = NO x (NO + NO 2 ) + any oxidized N with a single atom of N - NH x = NH 4+ + NH 3 - organic N 2. Unreactive - N 2 - N 2 O - organic N (soil) See tables.
46 Global N Patterns/budget (cont.) Table 1. Estimates of the active pools in the global nitrogen cycle (tonne = 1000 kg). million tonnes N Air Land Sea N N 2 O Plants Animals 200 of which people 10 Soil organic matter of which microbial biomass Plants 300 Animals 200 In solution or suspension of which NO 3- -N of which NH 4+ -N Dissolved N
47 Global N Patterns/budget (cont.) Table 2. Production of combined nitrogen gases by land, sea and air. Gas Atmospheric-stock, million tonnes N Residence time in atmosphere Annual production, million tonnes N per year NH 3 <1 6 days 54 ± 8 N 2 O years 14 ± 7 NO x <1 5 days 48 ± 15
48 Global N Patterns/budget (cont.) Preindustrial N budget The transfer of reactive to unreactive N was balanced. N 2, N 2 O produced by denitrification in oceans and soil. NH 3 is released by volatilization. NH 4+ = NH 3(aq) + H + ; pk a = 9.3 NH 3(aq) = NH 3(g) This process occurs only under high ph conditions. NH 3 is released by burning of plants. NH 3 is very reactive and has a short residence time in the atmosphere. NH 3 + H 2 O = NH 4+ + OH -
49 Global N Patterns/budget (cont.) NO can be formed by 1. Oxidation of N 2 by lightning; 2. Soil microbes; 3. Burning of biomass. NO, NO x are very reactive and have a short residence time in the atmosphere. In the preindustrial world, N inputs were largely retained where they were deposited. Nitrogen is a tightly conserved element in terrestrial environments because it is the growth limiting nutrient.
50 Global N Patterns/budget (cont.) NH 4+ - relatively immobile form of N a. Strongly assimilated by biota due to energetics; b. Abiotically retained on soil cation exchange sites. NO 3- - relatively mobile from of N a. No significant mechanism of abiotic retention. Nitrification is a key process regulating the mobility of N. Riverine fluxes of N are thought to be kg N/km 2 -yr and this is thought to largely occur as particulate organic N.
51 Global N Patterns/budget (cont.) Anthropogenic Sources Human activity has had a profound effect on the N cycle. Three processes largely contribute to this disturbance, through anthropogenic nitrogen fixation. 1. Energy production - under high temperature combustion processes, unreactive nitrogen is converted to reactive nitrogen by two processes. a. Thermal NO x 1000 o K N 2 + O 2 2NO b. Fuel NO x - the oxidation of organic N in fuels Natural gas - very low 0% Coal - up to 3% Both thermal and fuel NO x can be significant, but fuel NO x is often the dominant source.
52 Global N Patterns/budget (cont.) 2. Fertilizer-Most anthropogenic fertilizers are either NH 3 or urea produced from NH 3. This material is produced by the Haber process. 4N H 2 = 8NH 3 This is a very energy intensive process if natural gas is the energy source for H 2, as it usually is. 3CH 4 + 6H 2 O + 4N 2 = 3CO 2 + 8NH 3 3. Production of legumes and other crops allows for the conversion of N 2 to reactive N by increasing biological nitrogen fixation. Legumes include: Soybeans Ground nuts (peanuts) Pulses (lentils) Forage (alfalfa, clover)
53 Nitrogen Drivers in 1860 from J. Galloway presentation at Ammonia Workshop (NADP) October 22-24, 200, Washington, DC Grain Production Meat Production Energy Production
54 The Global Nitrogen Budget in 1860 and mid-1990s, TgN/yr NO y 8 5 N NH x Galloway et al., 2003b
55 Global Population and Reactive Nitrogen Trends Human Population (billions) 4 2 Natural N Fixation Tg N yr Population Haber Bosch C-BNF Fossil Fuel Total Nr From Galloway et al In review.
56 Nitrogen Deposition Past and Present mg N/m 2 /yr Galloway et al., 2003b
57 Nitrogen Drivers in 1860 & 1995 Grain Production Meat Production Energy Production
58 The Global Nitrogen Budget in 1860 and mid-1990s, TgN/yr NO y 8 5 N NH x mid-1990s NO y N NH x N 2 + 3H NH 3 Galloway et al., 2003b
59 Global N Patterns/budget (cont.) All three categories of anthropogenic nitrogen fixation have increased, but most significant is fertilizer consumption. The rate of fertilizer consumption is increasing particularly in Asia. There are two critical questions in response to this change. 1. What is the fate of this fixed N; and 2. What are the effects of this increase in fixed N?
60 IV. PATTERNS OF N AT THE HBEF (HBEF W6, CPW, BNA)
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67 moles N/ha-yr Bormann et al. (1977) Inputs Bulk Precipitation Dry Deposition N-fixation Total Inputs Outputs Streamwater DIN DON Denitrification 0 0 Total Outputs Changes in Pools Biomass Forest Floor Mineral Soil Net Retention
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Amino sugars 5-10% Purine and Pyrimidine Bases trace amounts. Undescribed Lots - non-protein N Crude proteins Lignin - N
N in Soil Note: soil concentrations can be anywhere, depending on vegetation, land use, etc. But a substantial amount indeed most (ca. 99%) soil nitrogen is organic Free amino acids trace amounts Amino
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