Marine Nitrogen Cycle Lecture 23:

Karen Casciotti

Overview

• Why study the nitrogen cycle?

• Nitrogen pools, fluxes, and distributions

• Biogeochemical transformations

• Open questions

• Human impacts on the nitrogen cycle

Life Needs Nitrogen

* *

*

C:N = 6.6N:P= 16:1

Overall Phytoplankton

C39H53O24N15P4

C:N = 2.6

C61H97O20N16

C:N = 3.8

30% chemical

70% H2O

% Wet Weight

Bacterial CellIons, small molecules (4%)

Phospholipids (2%)

DNA (1%)

RNA (6%)

Proteins (15%)

Polysaccharides (2%)

Mac

rom

olec

ules

Figure by MIT OCW.

Nitrogen transformations

Chemical species

Norg, NH4+

NH2OH

N2

N2O

NO

NO2-

NO3-

Oxidation state

-III

-I

0

I

II

III

V

Reduced

Oxidized

Marine Nitrogen Pools

• Nitrogen gas (N2) 95.2 % Nitrous oxide (N2O) Nitric oxide (NO)

• “Fixed” Nitrogen Inorganic nitrogen:

Nitrate (NO3-)

Nitrite (NO2-)

Ammonium (NH4+)

Organic nitrogen: Detritus and Living biomass Dissolved organic matter

• Proteins/Amino acids • Urea • Nucleic acids

2.5 %

2.3%

N2 Inorganic Organic

Sea Surface Chlorophyll a

Dugdale and Goering, 1967:the New Production paradigm

N2 fixation

Zooplankton

Bacteria Euphotic zone

Aphotic zone

NH4+

Export production NH4

+ Dead organic matterNO3 -

Nitrification

New Production Grazing

Phytoplankton

DON

Ammonification

Regenerated Production

Dugdale and Goering, 1967:the New Production paradigm

• Introduced the concept of balanced new andexport production

• Introduced the use of 15N-labeled compounds to measure rates of new andregenerated production.

• “Ammonium is an important nitrogensource… but nitrate and nitrogen fixationare the most important parameters withrespect to nitrogen limitation of primaryproductivity.”

Eppley and Peterson, 1979:Export Production and the “Biological Pump”

N2 fixation

Zooplankton

Bacteria Euphotic zone

Aphotic zone

NH4+

Export productionNH4

+ Dead organic matterNO3 -

New Production Phytoplankton

DON, DOC

Regenerated Production

CO2

+ CO2 + CO2

+ CO2

Atmosphericdeposition

Eppley and Peterson, 1979

• “Only the sinking flux due to newproduction associated with N2 fixation and atmospheric sources of N can beidentified as… transport ofatmospheric CO2 to the deep ocean.”

• Introduced “f ratio” as ratio of new/total production

Sea Surface Nitrate Map

Sea Surface Nitrate Map

‘HNLC’ regions(high nutrient, lowchlorophyll)

These regionsare typicallylimited byother factors: • Light • Temperature • Iron,micronutrients

Sea Surface Nitrate Map

Distribution of Nitrate in Atlantic Ocean

SOUTH NORTH

Nitrate section through the ETP

Redfield Ratios and Remineralization

“Redfield Ratio”: C106:N16:P1applies to both the average composition of

phytoplankton biomass and the ratio ofnitrate and phosphate generated from organic

matter remineralization under oxic conditions

Remineralization of generalized organicmatter: (CH2O)106(NH3)16(H3PO4) + 138 O2

106 CO2 + 16 HNO3 + H3PO4 + 122 H2O

(32 O2)(106 O2)

[µmol kg-1]

0.00.0

5.0 10.0 15.0 20.0 25.0 30.0 35.0 40.0 45.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Nitrate [µmol kg-1]

Phos

phat

e [µ

mol

kg-1

]

Figure by MIT OCW.

Global Thermohaline Circulation

SAMW & LOIW

SLW

NIIWBIW & RSW

CDW NADW

NA

DW

AABW

NADWNADW

LOIW

UPIW

SAMW

CDW

CDW

NPDW

LOIW

UPIWSAMW

SAMW & LOIW

IODW

ACCS

AUSTR.

JAVAINDIAN SOUTHERN OCEAN

ATLANTIC

INDONESIA PACIFIC

NORTH

NORTH

NORTH

SOUTH

SLW

SAMW

RSW

AABW

NPDW

ACCSCDW

NADW

UPIW

LOIW

IODW

BIW

NIIW

Surface layer water

Subantarctic mode water

Red sea water

Antarctic bottom water

North pacific deep water

Antarctic circumpolar current system Circumpolar deep water

North atlantic deep water

Lower intermediate water, 27.2 < σθ < 27.5_ _Upper intermediate water, 26.8 < σθ < 27.2_ _

Indian ocean deep water

Banda intermediate water

Northwest Indian intermediate water

From Pacific

Antarctica

Figure by MIT OCW.

Distribution of Nitrate in Atlantic Ocean

SOUTH NORTH

NADW AAIW

AABW

Overview

Why study the nitrogen cycle?

Nitrogen pools, fluxes, and distributions

• Biogeochemical transformations

• Open questions

• Human impacts on the nitrogen cycle

Microbial Nitrogen Cycle

Denitrification

state

Org NH3

NH2OH

NO2 -

NO

N2ON2

Nitrification

Nitrogen fixation

Assimilation

Anammox

NO3-

Nitrite oxidation

Oxidation Ammonia oxidation (-III) (-I) (0) (I) (II) (III) (V)

Overview

Why study the nitrogen cycle?

Nitrogen pools, fluxes, and distributions

• Biogeochemical transformations

• Open questions

• Human impacts on the nitrogen cycle

Redfield Ratios and Remineralization

“Redfield Ratio”: C106:N16:P1applies to both the average composition of

phytoplankton biomass and the ratio ofnitrate and phosphate generated from organic

matter remineralization under oxic conditions

Remineralization of generalized organicmatter: (CH2O)106(NH3)16(H3PO4) + 138 O2

106 CO2 + 16 HNO3 + H3PO4 + 122 H2O

(32 O2)(106 O2)

[µmol kg-1]

0.00.0

5.0 10.0 15.0 20.0 25.0 30.0 35.0 40.0 45.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Nitrate [µmol kg-1]

Phos

phat

e [µ

mol

kg-1

]

Figure by MIT OCW.

Sea Surface Nitrate Map

HOTS:N2 fixation may

account for 30-50% of export production

2Evidence for N Fixation

• Occurrence of nitrogen fixing species,such as Trichodesmium spp.

• Low δ15N of sinking organic mattersuggestive of significant N2 fixation

• Acetylene reduction or 15N2 incorporation rate estimates

Oceanic Diazotroph Diversity

Zehr, 2000Trends in Microbiology

Image removed due to copyright restrictions.

Water Column Denitrification Zones

Arabian Sea

Eastern TropicalNorth Pacific

Eastern TropicalSouth Pacific

Overview

Why study the nitrogen cycle?

Nitrogen pools, fluxes, and distributions

Biogeochemical transformations

• Open questions

• Human impacts on the nitrogen cycle

Major Questions inMarine N Cycling

• Is the nitrogen cycle in balance?

• How does the N cycle vary on glacial/interglacialtimescales?

• How is N2O produced in the ocean?

• By what mechanism is ‘extra excess N2’ formed?

Nitrogen Inputs to the Ocean

Nitrogen Atmospheric Continental

Fluxes in Tg N/yr

Fixation Deposition Runoff

Codispoti and 25 24 25Christensen [1985] Gruber and Sarmiento 125 ± 50 15 ± 5 41 ± 20[1997] (preindustrial) Gruber and Sarmiento 125 ± 50 30 ± 5 76 ± 20[1997] (postindustrial) Codispoti et al [2001] Same as G&S 86 Same as G&S

(includes DON)

Ocean Nitrogen Exports from the

Organic Sedimentary Water column Burial Denitrification Denitrification Anammox

Fluxes in Tg N/yr

Codispoti andChristensen [1985] 21 60 60 ? Gruber and Sarmiento [1997](preindustrial)

15 ± 5 85 ± 20 80 ± 20 ?

Gruber and Sarmiento [1997](postindustrial)

25 ± 10 95 ± 20 80 ± 20 ?

Codispoti et al[2001] 25 ± 10 300 150 ?

Nitrogen Budgets

Codispoti andChristensen

[1985]

Gruber and Sarmiento [1997]

Codispotiet al [2001]

Total sources 74 181 ±44 231 ±44 287

Total sinks 142 184 ±29 204 ±30 481

Residence time of N in the ocean

5,000 years 3,500 years 1,500 years

Is the N cycle in balance? Maybe not!Is it a moving target?

What are the consequences?

Major Questions inMarine N Cycling

• Is the nitrogen cycle in balance?

• How does the N cycle vary on glacial/interglacialtimescales?

• How is N2O produced in the ocean?

• By what mechanism is ‘extra excess N2’ formed?

Southern ocean nitrate utilization changes

Sigman et al., 1999

Higher δ15N in diatom-bound organic mattersuggests higherdegree of nitrateutilization in the Antarctic zone during glacialtimes.

00

10

20

30

40

50

60

70

80

900 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5

1 2 3 4 5 6 7 8 9 10 15 20 25 30 35 40 451050

15 20 25 30 35 40 451050

treated>63µmtraction

treateddiatoms

bulksediment

dept

h (c

m)

Depth profiles in gravity core All 107-22 (Antarctic Zone, Atlantic Sector, 55oS, 3oW, 2768 mi of (a) δ13N and (b) N content of bulkN (open circles), diatom N (solid circles), and the perchloric acid-treated >63 µm fraction (crosses). which is composed of large diatoms,radiolaria and some detrital gains, Replicate analyses are shown for the cleaned diatom and >63 µm fraction with solid line connecting the mean value of diatoms N analysis. The N content of the builk sediment is in some cases lower than that of diatorn fraction becauseof the presence of dense detrital grains in the bulk sediment the planktonic focaminiferal δ13 stratigraphy [from keigwin and Boyle, 1989]suggested that sediment from the last Glacial maximum is at 65 cm depth.

δ18o

N content (µmol N g-1 sediment)

δ18O (% vs. PDB)

δ15O (% vs. air)

Figure by MIT OCW.

Southern ocean nitrate utilization changes

Sigman and Boyle, 2000 Figure by MIT OCW.

Changes in Denitrification

Sedimentary δ15N changes from the ETNP

Chart removed due to copyright restrictions.Ganeshram, R., et al. "Glacial-interglacial Variability in Denitrification in the World’sOceans: Causes and Consequences." Paleoceanography 15, no. 4 (2000): 361–376.

Changes in Denitrification

Present LGM

N2 NO3 -

PN

High δ15N

High δ15N-PN

N2 NO3 -

PN

Lower δ15N

Lower δ15N-PN

Major Questions inMarine N Cycling

• Is the nitrogen cycle in balance?

• How does the N cycle vary on glacial/interglacialtimescales?

• How is N2O produced in the ocean?

• By what mechanism is ‘extra excess N2’ formed?

N2O vs. AOU

Yoshinari, 1976

Anticorrelation of N2O and O2 concentrations suggests N2O is producedduring organic matterremineralization (nitrification)

Figure by MIT OCW.

200

400600800

1000

2000

3000

4000

5000

200

400600800

1000

2000

3000

4000

5000

0

0

0.2 0.4 0.6 0.8 1.0 3 4 5 6 7

0.2 0.4 0.6 0.8 1.0 3 4 5 6 7

DEPTH (m)

DEPTH (m)

Vertical NO2 and O2 profiles at three different atations in the western North Atlantic, a, slope water of fNova Scotia (42o 18' N, 61o 24' W ); b, Gulf Stream (39o 07' N, 62o 21' W); c, Sargasso Sea (35o 52' N, 63o 44' W)

N2O µg/l

N2O µg/l O2 ml/l

O2 ml/l

October 1971July 1972

October 1971

July 1972May 1972

Nitrification

Ammonia-oxidizing nitrifiers:Nitrosomonas, Nitrosospira, Nitrosococcus

NH3 + 3/2 O2 NO2- + H2O + 2 H+

Nitrite-oxidizing nitrifiers:Nitrobacter, Nitrospira, Nitrospina

NO2- + 1/2 O2 NO3

-

NH3 + 2 O2 NO3- + H2O + 2 H+ Overall

Rates and Distributions

Chart removed due to copyright restrictions.Dore, J. E., B. N. Popp, D. M. Karl, and F. J. Sansone. "A Large Source of AtmosphericNitrous Oxide from Subtropical North Pacific Surface Waters." Nature 396, 63-66.

2Denitrification and N O

Chart removed due to copyright restrictions.Yoshinari, T., et al. "Nitrogen and Oxygen Isotopic Composition of N2O from Suboxic Watersof the Eastern Tropical North Pacific and the Arabian Sea—Measurement by Continuous-FlowIsotope-ratio Monitoring." Marine Chemistry 56 (1997): 253-264.

Major Questions inMarine N Cycling

• Is the nitrogen cycle in balance?

• How does the N cycle vary on glacial/interglacialtimescales?

• How is N2O produced in the ocean?

• By what mechanism is ‘extra excess N2’ formed?

Nitrate deficits

“N*” based on Redfield relationship of NO3- and PO4

3-: (CH2O)106(NH3)16(H3PO4) + 138 O2

106 CO2 + 16 HNO3 + H3PO4 + 119 H2O

N* = [NO3-] - 16 [PO4

3-] + constant

Denitrification: N* ↓ (lower [NO3-], unchanged [PO4

3-]) Also, higher N2/Ar because of N2 production from nitrate

production/accumulation of N2 yields “excess N2”

But, there’s more N2 than expected from nitrate deficits!!this phenomenon has been termed “extra excess N2”

“ ”Extra Excess N

What is it? • Discrepancy between N deficit based on N:P ratios andN2 excess from N2/Ar ratios

How could it be explained? • Remineralization of organic matter with high N:P ratio• Lateral mixing of N2 from sedimentary denitrification • Anammox

Anammox

NH4+ + NO2

- N2 + 2 H2O

Who: Bacteria in the order PlanctomycetalesWhat: anaerobically combine NH4

+ and NO2- to form N2

Where: anoxic sediments and watercolumns; Black Sea;Gulfo Dulce, Chile; Benguela Upwelling SystemWhen: ??Why: ??How: Anammoxosome; enzymology known incompletely,but genome sequencing is providing targets for biochemicalanalysis.

Measurement of Anammox

Anammox Isotopic tracers: 15N14NOrganic geochemistry: 15NH4

+ + 14NO2-

unique ladderane lipids

Molecular biology: Detection of anammox-type16S rRNA genes

Kuypers et al., Nature 2003

Isotopic Tracers of Anammox

MassesFor N2

14-14 14-15 15-15

15NH4+ 14NO3

- 14NH4+ 15NO3

-

Isotopic Tracers for Anammox

15N-NH4 addition

0

0.2

0.4

0.6

0.8

1

1.2

1 2 3

anammox1

denitrif1

15N-NO3 addition

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1 2 3

anammox2

denitrif2

14-14

14-14

14-15

14-15

15-15

15-15

Overview

Why study the nitrogen cycle?

Nitrogen pools, fluxes, and distributions

Biogeochemical transformations

Open questions

• Human impacts on the nitrogen cycle

Human perturbation of the Ncycle

"Natural" biological N fixation

Lightning

Fossil Fuel Combustion250

200

150

100

50

1920 1940 1960 1980Year

Glo

bal N

itrog

en F

ixat

ion

(Tg/

y)

Synthetic NFertilizer

Legume Crops andGreen Manures

Background

Anthropogenic

Nitrogen fixation byhumans is now equivalentto natural terrestrial nitrogen fixation (~140 TgN/yr).

The amount of human-produced N entering theoceans is not well known,but is on the order of 20-40 Tg N/yr

Figure by MIT OCW.

Eutrophication and Anoxia

Mississippi River nitrate loadsand Gulf of Mexico Hypoxia

Sea Surface Chlorophyll a