Transcript Biological control…

Weekly Theme: The Ocean as a Microbial Habitat
Daily Theme: Ocean biogeochemical variability
M J Perry Lecture: Biological control of ocean nutrients
C-MORE, 2 June 2010
What you should know by the end of lecture (at least something about):
What nutrients are controlled ?
Who’s doing the controlling ?
Why are they doing it ?
How do they do it ?
Gruber 2008
Upper ocean nutrient cycles
Dissolved
inorganic
nutrients
Uptake
(Drawdown)
N2
Particulate
organic
nutrients
Remineralization
(Recycling)
mixing
sinking
DON
remineralization and denitrification
at depth
Key biological transformations of elements (nutrients).
1) Uptake of dissolved inorganic nutrients and assimilation into
particulate organic nutrients
–
by autotrophs: phytoplankton and bacteria {little ‘b’ includes Archaea};
some heterotrophic bacterial uptake (e.g., NH4+), but won’t discuss today.
2) Consumption of organic particles by heterotrophs
– leads to synthesis of new organic compounds; still organic nutrient
3) Excretion of dissolved inorganic and organic nutrients
– as by-product of heterotrophic metabolism
3) Removal of nutrient from system
Sinking organic particles (long time to return), denitrification (permanent)
5) Change in bio-availability of nutrient – N2 fixation, chelation of
trace metals
Not all elements in seawater are considered as ‘nutrients’.
Major ions in seawater:
NaCl constitutes 85.65% of total
dissolved salts; together, six major
ions make up 99% of dissolved salts.
Cl -, Na+, Mg+2, SO4-2, Ca+2, K+
[mmol/kg range]
The major ions are mostly
conservative and are present in
~ constant proportions throughout
world oceans.
Neumann & Peirson 1966
5
Not all elements in cells are considered as ‘nutrients’.
Macro elements in cells – relative % of cell biomass
(in decreasing order; not including H2O):
C, H, O, N, P, S, Mg, K, Ca and Si (for diatoms, radiolarians)
Red elements are in low concentration in ocean (µmol/kg range),
in contrast to major salts on previous page (mmol/kg).
Micronutrients in cell – are minor % of mass, but
important:
Micronutrients are typically trace metals:
Fe+3 and Fe+2 – nanoM or sub-nanoM range
and other elements (Mn, Cu, Zn, Mo, Cd, V, Co, etc.)
Trace metals –> metaloproteins (electron transfer, enzyme catalysis).
Enzyme/cofactor requirements include Ferredoxin (Fe), carbonic
anhydrase (Zn), other trace metals…..
6
Seawater – top 6 ions
Plankton – top elements
Cl 546 mmol/kg
Na+ 469 mmol/kg
Mg+2 52.7 mmol/kg
SO4-2 28 mmol/kg
Ca+2
10.3 mmol/kg
K+
10.2 mmol/kg
C (DIC) 2.2 mmol/kg
C, H, O, N, P, S, Mg, K, Ca
and Si; concentrations lower
at surface:
NaCl constitutes 85.65% of
total dissolved salts.
These six major ions make
up 99% of dissolved salts.
N < 40 mol/kg
P < 3 mol/kg
Si < 150 mol/kg
Trace metals
[<nmol/kg]
Elements in red can be
limiting nutrients – limiting
both to phytoplankton
biomass and growth rate.
Key biological transformations of elements (nutrients).
I) Uptake of dissolved inorganic nutrients by autotrophs
(phytoplankton, bacteria) leads to assimilation of nutrients into
organic compounds. Increase in cell biomass leads to synthesis
of new cells. Drawdown of nutrient is flip side of uptake.
Waniek. 2003. J. Mar. Syst. 39:57 (spring bloom)
North Atlantic spring bloom observed from a float,
shows nitrate drawdown and chlorophyll increase from
mid April to late May 2008.
Chlorophyll
Nitrate
Bagniewski et al., in prep.
1a) Nutrient uptake has been described by
Michaelis Menton enzyme kinetics.
Paasche (1973)
Vmax
V
Vmax
S
KS
S0
KS
= uptake rate (mole/cell/time
= maximal rate
= concentration (mol/kg)
= substrate concentration
at 0.5 Vmax
Si concentration
N
Uptake rate ~ function of:
*nutrient concentration at cell surface (DIN;
related to cell size and relative motion),
* number/types of transporter (dots),
* internal concentration of nutrient (N), and
* growth rate (metabolic need).
Parameters vary w/ size, species, methodology.
Nutrient acquisition is affected by size:
concentration vs. distance from cell surface.
Steeper gradient for small cells - diffusion alone not so bad (PS bacteria)
Swimming or sinking improves flux; as
does other interactions with flow field
1b) Nutrient concentration can regulate growth rate
(shape of curve similar to uptake kinetics; KS for growth).
Growth
rate
Nutrient concentration
Culture data of Sommer
Nutrient could be N, P, Si, Fe, Zn, etc.
Nutrient concentration can regulate growth rate,
but real world relationships rarely looks like cartoon.
Growth
rate
Nutrient concentration
Goericke (2002)
Limnol. Oceanogr., 47: 1307
Nitrate and growth rate of specific phytoplantkon in Arabian Sea.
Nutrient concentration does not tell the whole story.
Ambient concentrations of nitrate do not reflect nutrient flux (from
mixing, diffusion or recycling through heterotroph excretion).
At low concentrations growth rate may be limited –– but if flux is large
enough, growth rate may NOT be nutrient limited.
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Goericke (2002) Limnol. Oceanogr., 47: 1307
1c) Internal nutrient concentrations may be a better
predictor of growth rate
(also note that shape of curve similar to uptake kinetics).
growth rate (doublings d- -1)
Problem -- internal concentrations are difficult to measure
10 -12 g N per cell
Mimimal requirement for structural cell components
Valiela, 1995; data of Goldman and McCarthy, 1978)
But . . . new single-cell techniques help quantify internal
concentrations for some elements.
diatoms
picophyto
heteroflag.
False-color X-ray fluorescence of Fe
in silicoflagellate – Southern Ocean
Twining et al. 2008. J. Eukaryot. Microbiol. 55: 155
Single-cell element data from preceding figure.
Units are µmole / liter cell volume
Twining et al. 2004. Limnol. Oceanogr. 49: 2115
1d) Nutrient concentration sets upper limit to biomass.
El Nino
Phytoplankton
biomass
Nutrient
concentration
Nutrient could be N, P, Si, Fe, Zn, etc.
La Nina
The actual biomass produced may be different – if other nutrients
are at limiting concentrations or if environmental conditions are
suboptimal (Fe - for example, HNLC regions, light, temperature, ).
Phytoplankton
biomass
Nutrient
concentration
Chlorophyll (~ biomass) vs. DIN concentration
http://www.ozcoasts.org.au/indicators/water_column_nutrients.jsp
The accumulated biomass may be less than observed – due to loss
after production (grazing, sinking, conversion to dissolved organics, ?)
Nitrate drawdown converted to POC (Redfield)
Beam attenuation converted to POC
D’Asaro et al. – Lagranian float in 2008 North Atlantic Bloom
1e) Can one predict drawdown of one nutrient from
drawdown in another?
Nitrate
Carbon
Redfield ratio (1963)
– empirical/statistical
relationship of molar
average elemental ratios
Alfred Redfield
Biological Redfield ratio C: N: P ~ 106: 16: 1
average molar elemental composition of particles (organisms)
Geochemical Redfield ratio C: N: P ~ 105: 15: 1
deep-water ions: nitrate, phosphate, and non-calcite DIC
106 CO 2  122 H2 O +16 HNO3  H3 PO4

(CH2 O)106 +(NH3 )16 +H 3PO4 +138 O2
autotrophy <–> heterotrophy connection
(autotrophy creates organics, respiration remineralizes nutrients)
C:P
The biological Redfield ratio has
taxonomic variability.
Co-evolution of organisms
& ocean chemistry
N:P
C:N
C:N:P composition varies between
phyla and superfamilies.
Phytoplankton C:P, N:P and C:N (mol:mol)
ratios are grouped phylogenetically –
Prasinophyceae (Prasino) and
Chlorophyceae (Chloro) are members of
the green (G) plastid superfamily
whereas Dinophyceae (Dino),
Prymnesiophyceae (Prymn) and
Bacillariophyceae (Diatoms) are members
of the red (R) plastid superfamily. Error
bars indicate standard errors.
Quigg et al. 2003. Nature 425:291
Redfield ratio has physiological variability.
Structural cell components
Growth- related N:P
Nutrient acquisition N:P
Storage N:P
see figure below
P-rich RNA  low N:P ratio
N-rich enzymes high N:P ratio
P can be stored if N is limiting
Structural N:P ratio of 29
species of freshwater and
marine phytoplankton.
0
48
Structural N:P ratio
Redfield ratio is shown, as is
the theoretical range predicted
by the model under 3 cases:
exponential growth (Opt exp),
competitive equilibrium with
light, N- and P- limitation.
Klausmeier et al. 2004 Nature 429: 171
Redfield ratio is changed by nutrient limitation.
1,600
For a cell limited by P,
relative concentration of other
elements in the cell will
increase:
When P is not limiting (far
right), growth rates can be
maximal.
C:P
N:P
120
When P is limiting (left), growth
rates are lower.
Growth rate, 26d-1
Redfield did not derive a ratio for trace metals,
but others have.
(Used in estimating Fe-fertilization carbon credits).
Stoichiometry shows (Ho et al, 2003, J. Phycol. 39: 1145)
taxonomic patterns related to evolution,
greater variability for metals that substitute in metaloenzymes
(e.g., Zn, Co, Cd),
reflects biogeography (coastal vs. oceanic).
Others studies show some phytoplankton can synthesize nonmetalo co-factors under Fe limitation or store Fe (ferritin) after an
Fe pulse.
Ho et al, 2003, J. Phycol. 39: 1145
http://www.awi.
de/fileadmin/us
er_upload/News
/Press_Releases/
2004/1._Quarter
/Thalassiosira_w.
jpg
Diatoms have a unique requirement for Si
(as do radiolarians). Ratios of diatom Si to other
elements vary.
Average Si: N ratio of 27 species = 1.05.
But >10-fold variation (p.3 to 4) independent of
variable growth conditions or nutrient availability.
(Brzezinski, 1985, cited in Marchetti & Cassar, 2009. Geobiology 7: 419
Si limiting
Martin-Jézéquel et al. 2002 J. Phycol. 36: 821
Si not limiting
Fe-limited
diatoms have
thicker frustules
(sink faster;
more resistant
to dissolution;
what’s impact
on Si cycle?
Key biological transformations of elements (nutrients).
1) Uptake of dissolved inorganic nutrients and assimilation into
particulate organic nutrients – by autotrophs: phytoplankton and
bacteria {little ‘b’ includes Archaea}; some heterotrophic bacterial uptake
(e.g., NH4+), but won’t discuss today.
2) Consumption of organic particles by heterotrophs
– leads to synthesis of new organic compounds; still organic nutrient
3) Excretion of dissolved inorganic and organic nutrients
– as by-product of heterotrophic metabolism
(some organic excretion by autotrophs under certain circumstances)
3) Removal of nutrient from system
Sinking organic particles (long time to return), denitrification (permanent)
5) Change in bio-availability of nutrient – N2 fixation, chelation of
trace metals
From a heterotroph’s perspective, organic particle
consumption leads to growth and reproduction.
But consumption is not efficient. Nutrients are released –
particulate organic, dissolved organic, and dissolved inorganic.
Consumption
Assimilation
Defecation &
sloppy feeding
Respiration
PON
(energy for
maintenance,
biosynthesis,
activity, etc.)
DIN and DON
Growth & Reproduction
Molt
PON
The more trophic transfers,
the more remineralization.
In the Microbial Loop, it’s almost all trophic transfers, so
recycling of nutrients is efficient.
(Net production of new POC is not efficient.)
DIN
Picoautotrophs
DOC
lysis
Microbial Loop:
DOC
POC
DIC
DIN
PON
DIN
HNF and ciliates have
v. high respiration rates
33
Where are
the gellies?
34
Heterotrophic Prokaryotes
* Sink for dissolved organics
(organics excreted by autotrophs, products of viral lysis,
inefficient zooplankton feeding, prokaryotic exoenzymes)
* Sink or source of dissolved inorganic nutrients?
[depends on the C:N:P ratio of dissolved organics]
Heterotrophic Protists
* Sink for particulate organics (ingest mostly small
bacterial-sized particles; repackage them into larger particles)
* Source of dissolved inorganic nutrients to
phytoplankton AND bacteria
(excretion or remineralization or regeneration of N, P, Fe, etc.
by virtue of their very high metabolic rates)
* Enhancement of food quality for mesozooplankton
35
How much C, N, etc. are remineralized?
Are bacteria remineralizers? or are they consumers of N ?
(same analogy for P, Fe, etc.)
Depends on the
quality of DOC
Low C/N;
low BGE
more C -> CO2
little N recycled
High C/N:
high BGE
more C -> biomass
more N recycled
Kirchman, Microbial Ecology of the Oceans
Key biological transformations of elements (nutrients).
1) Uptake of dissolved inorganic nutrients and assimilation into
particulate organic nutrients – by autotrophs: phytoplankton and
bacteria {little ‘b’ includes Archaea}; some heterotrophic bacterial uptake
(e.g., NH4+), but won’t discuss today.
2) Consumption of organic particles by heterotrophs
– leads to synthesis of new organic compounds; still organic nutrient
3) Excretion of dissolved inorganic and organic nutrients
– as by-product of heterotrophic metabolism
(some organic excretion by autotrophs under certain circumstances)
3) Removal of nutrient from system
Sinking organic particles, vertically migrating zooplankton, denitrification
5) Change in bio-availability of nutrient – N2 fixation, chelation of
trace metals
Sinking organic material (zooplankton fecal pellets, dead
zooplankton and fish, phytoplankton aggregates) removes
nutrients from the euphotic zone.
WHOI sediment trap collections
Particle aggregation and sinking.
http://www.whoi.edu/oceanus/viewArticle.do?id=2372
Burd & Jackson, 2009. Ann. Rev. Mar. Sc.
Organic material is consumed and nutrients are
remineralized if particles slowly sink. Subsurface oxygen
minimum is a signature of respiration.
Oxygen (µmol/kg)
Martin et al. 1987
Johnson,
http://www.mbari.org/chemsensor/pt
eo.htm
Diel and seasonal migration of zooplankton can
transport nutrients out of euphotic zone.
http://www.sintef.no/project/calanus
/graphics/calanus.jpg
Longhurst and Harrison. 1988. Vertical nitrogen flux from
the oceanic photic zone by diel migrant zooplankton and
nekton. Deep-Sea Res 35: 881.
Polyphosphate synthesis by diatoms may play a role in
permanent removal of P from the recycling pool.
(Organic phosphonates may sequester P for specific groups.)
http://www.bo
ne.pentax.jp/ne
wceramics_e.ph
p
In sediment, diatom
polyphosphate
enables transition to
apatite (crystalline
phosphorus calcium
deposit)
Diaz et al. 2008. Science 320: 652
Phosphonate use
by Trichodesmium
(Dave Karl lecture)
Denitrification removes bio-available from the ocean.
(and decreases the Redfield N:P ratio.)
Net effect is removal of available N
from ocean in anaerobic conditions:
Denitrification – when O2 is low, some
bacteria can use NO3- as a terminal
electron acceptor (use nitrate as a
substitute for oxygen). Heterotrophic.
NO3− → NO2− → NO + N2O → N2
Anammox (ANaerobic AMMonium
Oxidation). Autotrophic.
NH4+ + NO2− → N2 + 2H2O
There is more residual PO4-3, so
N:P ratio decreases.
Tyrrell, 2001
42
Key biological transformations of elements (nutrients).
1) Uptake of dissolved inorganic nutrients and assimilation into
particulate organic nutrients – by autotrophs: phytoplankton and
bacteria {little ‘b’ includes Archaea}; some heterotrophic bacterial uptake
(e.g., NH4+), but won’t discuss today.
2) Consumption of organic particles by heterotrophs
– leads to synthesis of new organic compounds; still organic nutrient
3) Excretion of dissolved inorganic and organic nutrients
– as by-product of heterotrophic metabolism
(some organic excretion by autotrophs under certain circumstances)
3) Removal of nutrient from system
Sinking organic particles, vertically migrating zooplankton, denitrification
5) Change in bio-availability of nutrient – N2 fixation, chelation of
trace metals
Trace metals are complexed by different classes of
organic ligands. Different ligands appear to give selective
advantage to different taxanomic groups.
Stronger class of chelator. Include
siderophores. Cyanobacteria are
able to access trace metal.
Eukaryotes are less able.
Weaker class of chelator. Thought
to be detrital in nature. Metal is
more accessible to eukaryotes.
Hutchins et al. 1999 . Nature 400, 858
N2 fixation adds bio-available N to the ocean.
(and increases the Redfield N:P ratio).
N2 + 6 H+ + 6 e− → 2 NH3
More Fe input to Sargasso Sea –> more N2 fixation –> higher N:P ratios.
Wu, Sunda, Boyle, Karl (2000.
Science 289: 759) suggest
Aeolian Fe (increases N through
N2 fixation.
(There is also a shift to N2-fixing
cyanobacterial species.)
Redfield ratio BATS vs. HOTS
Is the Redfield ratio still useful?
(it does vary)
106 CO 2  122 H2 O +16 HNO3  H3 PO4

(CH2 O)106 +(NH3 )16 +H 3PO4 +138 O2
Yes – some predictive power (e.g., ~ C fixed per N; eutrophication)
Yes – insight into autotrophy <–> heterotrophy connection
(elements are incorporated into organics and released or remineralized)
Yes – sight into opposing biological processes in nitrogen cycle:
N2 fixation adds N and denitrification removes N from ocean
Key biological transformations of elements (nutrients).
1) Uptake of dissolved inorganic nutrients and assimilation into
particulate organic nutrients
–
by autotrophs: phytoplankton and bacteria {little ‘b’ includes Archaea};
some heterotrophic bacterial uptake (e.g., NH4+), but won’t discuss today.
2) Consumption of organic particles by heterotrophs
– leads to synthesis of new organic compounds; still organic nutrient
3) Excretion of dissolved inorganic and organic nutrients
– as by-product of heterotrophic metabolism
3) Removal of nutrient from system
Sinking organic particles (long time to return), denitrification (permanent)
5) Change in bio-availability of nutrient – N2 fixation, chelation of
trace metals