N2 fixation/New production

Margie Mulholland

1Department of Ocean, Earth & Atmospheric Sciences

Old Dominion University

N2 fixation and C productivity

• Ultimately all new production is from N2 fixation. N limitation of primary productivity in the bulk of the ocean

• Fix new N into N limited aquatic systems to fuel ecosystem production

• N losses exceed N inputs in current N budgets – missing N2 fixation relative to denitrification?

• Changes in oceanic N inventory over time affects ocean productivity

Global distributions of diazotrophs

• How do we know where they are?

• Based on what’s known or thought about physiology

• Temperature

• Nutrient concentrations – absence of N, presence of Fe and P

• Ratios – geochemical inventories

• Satellites – ocean color and unique cyanobacterial pigments

Factors Potentially Limiting Marine N2 Fixation

• Physical: – light (photoautotrophs), – temperature – stability (mixing)

• Chemical: O2 (inhibition)• Nutritional: Fe, P, Si, Mo, other

metals; presence of DIN• Organic matter supply (heterotrophs)

Temperature - 20 degree isotherm

Trichodesmium focused

Moore et al. 2002

Nutrient limitation of N2 fixation

N2 fixation and dissolved Fe

Figure 3. Seasonal maps showing the potential for nitrogen fixation in the world oceans. Maps were generated by converting global dust iron fluxes to total dissolved iron and using the relationship shown in between log[Fe’] and nitrogen fixation : maximum nitrogen fixation. From Berman-Frank et al. 2001 (Fig. 6).

Global Trichodesmium bloom occurrence

• From Westberry and Siegel (2006)• 6-year mean (Sep 1997-Dec 2003)

Quantifying N2 fixation and N2 fixation from blooms

•Using 1500 mmol N m-2 d-1 for bloom N2 fixation rates (after Capone et al., 2006)

this depends on rate per colony usedalso on density of Tricho per literalso their physiological state

•“Normal” range of water column N2 fixation 15-691 mmol N m-2 d-

1 (Mulholland & Lomas 2008, Mulholland et al. 2006)•1000 mmol N m-2 d-1 during a Richelia bloom (Subramaniam et al. 2008)

Global Tricho bloom N2 fix = 8.5 ± 1.2 Tg N yr-1

• Total oceanic N2 fixation ~ 100 Tg N yr-1 (Galloway et al. 2004)– Range is 5 – 150 Tmol N yr-1 (Carpenter & Capone 2008)– depends on model used & drivers (which limitations are assumed)

• Basin-specific estimates also have order(s) of magnitude variability

• Not many measurements – need measurements for models!• Mostly Trichodesmium-based estimates – high variability in

rates of N2 fixation (0.1 – 20.4 nmol N col-1 d-1) and variable density, C:N2 fixation (1.2 – 703; is this physiology?) and N release rates (12-74% of recently fixed N2) (Mulholland et al. 2006, Mulholland 2007)

Context

~130 TgN/yr(40o S-65o N)

From Deutsch et al. (2007)

Global Geochemical N2 Fixation[m

mol/m

2/yr]

• Trichodesmium• Diazotrophic diatom associations (e.g.,

Richelia/Hemiaulus and others)• Coccoid cyanobacteria (groups a, b, and c)• Bacterioplankton- & proteobacteria• Copepod gut flora• Archaea

Other pelagic sources of N2 fixation:

Moisander et al. 2010

UCYN-A

Crocosphaera

18 & 25 oC isotherm

Other diazotrophs might have broader ranges

Global “Cyanobacteria” distribution

• Yellow = Synechococcus-like cyanobacteria (SLC)

From Alvain et al. (2008)

Deutsch et al. 2007

Assume flux associated with fixation

C Flux from Dinitrogen Fixation

Lower euphotic

zone- 100 -

(Chl max)PONNO3

-

Uppereuphotic

zone

N2 fixation

Classical viewView with N2 fixation

Desert

PON/POC

DIC/NH4+ PON/POC

100- 0 -

- 50 -

- 75 -

- 25 -

De

pth

(m)

CO2

CO2

NO3-/

DIC

PONNO3-

NH4+

CO2

N2

PON/POC

NO3-/

DICPON/POC

More new production = greater export productionBut does this account for the ecology?

PON/POC

PON/POC

DIC/NH4+ PON/POC

NO3-/

DIC

Up

per

eu

ph

oti

c zo

ne

Lo

we r

eu

ph

oti

c zo

ne /

chl

max

CO2

PON/POC

DIC/NH4+

N2

PON/POC

NO3-/

DICPON/POC

CO2

PON/POC

DIC/NH4+ PON/POC

NO3-/

DICPON/POC

NO3-/ CO2NO3

-/ CO2NO3-/ CO2

A. Classical gyres B. N2 fixation & export C. N2 fixation & remineralization

OR

OR

CO2N2

Hood et al. 2000, Mulholland 2007

Implications?Does N2 fixation yield stoichiometric drawdown of atmospheric CO2?

Sinking

Trichodesmium

Grazers

TrichodesmiumOR

MicrobialLoopPhyto

NH4+ & DON & DOCVirus

Ecology matters

Subramaniam et al. 200?

Implications?Maybe for some N2 fixers?

Sinking

DDA’s?

Grazers

TrichodesmiumOR

MicrobialLoopPhyto

NH4+ & DON & DOCVirus

What about picocyanos?

The fate of new N in tropical systems

Alternative hypotheses:

1. New N from nitratenet autotrophy

sinking of large cells

grazing by large copepods

Large particle flux

No microbial loop

2. New N from N2 fixationnet heterotrophy

release of recently fixed N2

microbial remineralizationhigh DOM flux

Little particle flux

Developed microbial loop

Trophic transfer of fixed N

Correlation between timing and magnitude of blooms of Karenia brevis and Trichodesmium spp. in GOM and coastal Atlantic

Results from CliVEC

• High N2 fixation rates in unexpected places (coastal systems)

• Diverse diazotrophs in coastal systems

Other observations:

• Chl a not always well-correlated with productivity

• C and N productivity are not well correlated

High rates of coastal N2 fixation in coastal Atlantic

• N2 fixation rates were not correlated with temperature

• Higher rates in colder water

• Areal and volumetric rates comparable to oceanic rates

High rates of areally integrated N2 fixation rates (Aug 2009)

Range of 17.0 – 715mol N m-2 d-1

N2 fixation rates were not confined to warm waters

High N2 fixation not focused in high Chl areas

Depth integrated N2 fixationmol m-2 d-1 on Chl

Aug 09

Areal rates of N2 fixation

• Areal rates 36.7 to 340 mol N m-2 d-1 in Summer and 32.7 to 199.6 mol N m-2 d-1 in Fall

• Areal rates for tropical and subtropical oceans range from 3.7 to 703 mol N m-2 d-1

• Areal rates for tropical North Atlantic Ocean average 239 mol N m-2 d-1

• English channel (2 sites) 350 mol N m-2 d-1 in summer

Annual rates of N inputs due to N2 fixation

• Seasonally and between 35-45oN, an area 6.4% of the North Atlantic continental shelf

• Use our average of 135.1 mol N m-2 d-1

• N input is 0.02 Tmol N y -1, the amount previously calculated for the entire North Atlantic continental shelf (Nixon et al. 1996)

• If this rate applies for the whole shelf then 0.31 Tmol y -1 is input from shelf N2 fixation

• Estimates of N2 fixation for the entire N Atlantic basin are 0.15 to 6.4 Tmol N y -1

• This is about 10% of the estimated N removal due to denitrification for the same area

• How widespread is coastal N2 fixation???

Distribution of nif groups - qPCRGroup a – UCYN-A

Unknown

Group b (DNQ)

TrichodesmiumHemi/Richelia

2.5 – 3.5 x 107 nif gene copies for UCYNA; very high!

High Tricho nif abundance and DDAs in 2006

4.3 – 6.5 x 106 nif genecopies for UCYNA

Tricho detected

UCYNA & DDAs104 - 106

Who and where were the diazotrophs?

Range of 11.4 – 275.2

mol m-2 d-1

Tricho quantifiable

UCYN-AUCYN-A

Hemi/RicheliaHemi/Richelia

UCYN-AUCYN-A

UCYN-A are dominant• UCYN-A were

the dominant diazotroph detected with qPCR (x106 gene copies)

• Among highest gene copies observed

Primary productivity (mmol C m-2 d-1) and SST(not correlated to N2 fixation)

Depth integrated C fixationon SST; Range 11.2 – 209.4 mmol m-2 d-1

Aug 09

Depth integrated C fixationmmol m-2 d-1 on ChlRange 11.2 – 209.4

Aug 09

Primary productivity (mmol C m-2 d-1) and Chl

Summary• The mid-Atlantic shelf harbors a diverse group of

diazotrophs which fix N2 at high rates (bacteria have low 15N there although diazotrophs were not observed in Meador study)

• Coastal areas are largely excluded from geochemical estimates on the grounds that they are nutrient replete.

• We are really in our infancy in understanding where N2 fixation occurs and the physiological capacity and limitations of diazotrophic organisms.

Implications for C

• N2 fixation related to new production and fluxes

• New production underestimated

Many other complications:• But UCYN-A are photoheterotrophs so may not

fix or draw down C• Food web interactions

• Future scenarios with high CO2?

Future• Increased N2 fixation - ~25 -

50% with doubled pCO2 affecting ecosystems and C export

• Increases in Tricho and other cyanos ranges with warming

• Increased N release fueling regenerated production

• Which taxa will respond?• In food webs and

biogeochemical function and ocean C uptake, not all phytoplankton are equal

Hutchins, Mulholland, & Fu 2009

0

100

200

300

400

500

600

N2 f

ixat

ion

(n

mol

N L

-1 h

-1) 380 ppm

750 ppm

10/26/0710/24/07 10/25/07

(nm

ol N

mg

Ch

l a-1

hou

r-1 )

0

2

4

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14IMSChl a-normalized

ControlHigh temperatureHigh CO2

Greenhouse

GBRCell-normalized

(nm

ol N

cel

l-1

hou

r-1 )

0

1x10-6

2x10-6

3x10-6

4x10-6

5x10-6

6x10-6

IMSCell-normalized

GBRChl a-normalized

Other diazotrophs

• Yes for Crocosphaera

• Working on others

• Effect of other climate change variables on diazotrophy? Stratification? etc

• Expanding ranges of diazotrophs and cyanos in general?

• Other changes in phytoplankton communities in general?

The Future

• Difficult to assess changes over time because of variability and we don’t know the physiological diversity of most diazotrophs (Tricho won’t grow at 180ppm)

• More measurements from the coastal region here and elsewhere to better resolve variability in C and N2 fixation

• Better understanding of the physiology of the diverse group of diazotrophs and their limits and tolerances to advise models

• Need to understand mechanisms to be predictive

Needs• Where is N2 fixation? Where isn’t it? (e.g., eastern Med – models

predict N2 fixation; Yogev et al. 2011, Mulholland & Capone 2009)

• What N2 fixers are where? What is their physiology and role in ecosystem production?

• Relationship of diazotrophic production with export (grazing on diazos)• Relationship of diazotrophs within ecosystems – ecosystem balance (net

auto vs. net hetero) • Ecosystem shifts over time associated with climate variability and

change• Nitrogen:carbon relationship

Physiology

• Important

• Can’t capture it all in models

• What are the most important physiological characteristics to get right?

• To describe the past?

• To project the future? (the goal)