the Fe nucleus, thus decreasing d. In contrast, the
removal of an electron from the redox-active
ligand orbital has a minor effect on d (e.g., d =
−0.15 mm/s for [FeIV(B*)+•(O)]− compared
with d = −0.12 mm/s for [FeIV(B*)(O)]2−) (table
S5). Inspection of the DFT results shows that
the Fe-O bond of 3 has nearly the same covalency as the Fe-O bonds in FeIV=O complexes
(12, 17, 18). The calculated unpaired spin density
on the oxo group of 3 is 0.22, which is less than
expected (≈0.4) by comparison with FeIV=O complexes (≈0.8); the difference can be traced to a
spin polarization of the bonding (px + dxz) orbital.
The exchange potential generated by the dayz
electron places the virtual daxz level below the
dbxz level. As a consequence, the transfer of electron density from pax to daxz is greater than from pbx
to dbxz , resulting in a negative spin density in px,
which, combined with the positive spin density for
py (~0.4), yields a net spin density of less than 0.4.
The z axis of Eq. 1 parallels the Fe-O bond
within 5°. The unpaired electron in the dyz orbital
produces a large negative x component of the
spin-dipolar part of the A tensor, A(s-d)i/gNbN =
(−24.4, +8.7, +15.7) T, and together with the
isotropic contact term gives the larger A value
along x. Owing to the large energy gaps between
the narrowly spaced (dxz, dyz) pair and the other
3d levels, spin-orbit coupling acts primarily
between dxz and dyz and produces (i) an effective
g value gz = 2(1 – ζ/D) (gx and gy are not affected) and (ii) an orbital contribution to the mag-
netic hyperfine interaction, ALzIzSz, where ALz =
P(gz − 2) ≈ −13 T. Substitution of ζ = 260 cm–1 and
DDFT = 2000 cm–1 gives the observed value gz =
1.74 and ALz = −13 T (19).
Complex 3 thus appears to have a low-spin d3
configuration in contrast to a recently described
isoelectronic manganese(IV)-oxo complex (20),
which is high spin, S = 3/2, by EPR criteria. Our
particular interest in TAML-catalyzed reactions
pertains to their proven potential in green chemistry. The present work provides an opportunity to
elucidate elementary steps in the catalytic cycles of
TAML activators by taking advantage of the high
purity of 3, with its various prominent spectroscopic signatures, as a stoichiometric reagent.
References and Notes
1. I. G. Denisov, T. M. Makris, S. G. Sligar, I. Schlichting,
Chem. Rev. 105, 2253 (2005).
2. E. I. Solomon et al., Chem. Rev. 100, 235 (2000).
3. M. Costas, M. P. Mehn, M. P. Jensen, L. Que Jr., Chem.
Rev. 104, 939 (2004).
4. D. N. Harischandra, R. Zhang, M. Newcomb, J. Am. Chem.
Soc. 127, 13776 (2005).
5. M. Newcomb et al., J. Am. Chem. Soc. 128, 4580 (2006).
6. N. Aliaga-Alcalde et al., Angew. Chem. Int. Ed. 44, 2908
(2005).
7. A. Chanda et al., J. Inorg. Biochem. 100, 606 (2006).
8. A. Ghosh et al., J. Am. Chem. Soc. 127, 2505 (2005).
9. D. Banerjee et al., Angew. Chem. Int. Ed. 45, 3974 (2006).
10. S. S. Gupta et al., Science 296, 326 (2002).
11. M. J. Bartos et al., Coord. Chem. Rev. 174, 361 (1998).
12. M. R. Bukowski et al., Science 310, 1000 (2005).
13. J.-U. Rohde et al., Science 299, 1037 (2003).
14. Materials and methods are available as supporting
material on Science Online.
Small Phytoplankton and Carbon
Export from the Surface Ocean
Tammi L. Richardson1* and George A. Jackson2
Autotrophic picoplankton dominate primary production over large oceanic regions but are believed
to contribute relatively little to carbon export from surface layers. Using analyses of data from
the equatorial Pacific Ocean and Arabian Sea, we show that the relative direct and indirect
contribution of picoplankton to export is proportional to their total net primary production, despite
their small size. We suggest that all primary producers, not just the large cells, can contribute
to export from the surface layer of the ocean at rates proportional to their production rates.
arbon export from the oceanic surface
layer is controlled by biological transformations that occur within the pelagic
food web (1, 2). Autotrophic picoplankton (<2 mm
in diameter) often dominate primary production
in these regions but are believed to contribute
relatively little to carbon export from surface layers because of their small sizes, slow sinking
rates, and rapid utilization in the microbial loop.
C
1
Marine Sciences Program and Department of Biological
Sciences, University of South Carolina, Columbia, SC
29208, USA. 2Department of Oceanography, Texas A&M
University, MS 3146, College Station, TX 77843–3146,
USA.
*To whom correspondence should be addressed. E-mail:
[email protected]
838
Large, rapidly sinking phytoplankton, such as
diatoms, are believed to control carbon flux
from upper ocean layers, and their contributions to export are believed to be disproportionately larger than their contributions to total
primary production (1). Here we ask whether the
contributions of picoplankton to carbon fluxes
from the surface ocean are, in fact, disproportionately low.
Using results from inverse and network
analyses of U.S. Joint Global Ocean Flux Study
(JGOFS) data from the equatorial Pacific (EqPac)
and Arabian Sea, we show that the relative
contributions of various phytoplankton size
classes to carbon export are proportional to their
contributions to total net primary production
(NPP) (3) (Fig. 1). Potential export pathways
9 FEBRUARY 2007
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15. The 3d spin-flip transition (dxy)b → (dxz)a is higher in energy
than the ligand-to-metal transition (pp)b → (dxz)a, where pp
is the redox-active orbital of the phenyl moiety, owing to the
large {dxz, dyz} − dxy splitting.
16. J. T. Groves, J. Inorg. Biochem. 100, 434 (2006).
17. A. Decker, M. D. Clay, E. I. Solomon, J. Inorg. Biochem.
100, 697 (2006).
18. F. Neese, J. Inorg. Biochem. 100, 716 (2006).
19. The free-ion value for the one-electron spin-orbit coupling
constant z is 580 cm–1 (21). Given the high degree of
covalency of 3, the adopted z is not unreasonable. P = 2 gN b
bN <r–3>3d has been taken as 50 T.
20. T. H. Parsell, R. K. Behan, M. T. Green, M. P. Hendrich,
A. S. Borovik, J. Am. Chem. Soc. 128, 8728 (2006).
21. J. Bendix, M. Brorson, C. E. Schaffer, Inorg. Chem. 32,
2838 (1993).
22. The work was supported by NIH grants EB001475 (E.M.)
and GM-38767 (L.Q.), the Heinz Endowments (T.J.C.),
Environmental Protection Agency (grant RD 83 to T.J.C.),
and the Heinz Foundation for the Teresa Heinz Scholars
for Environmental Research award (to D.B.). XAS data
were collected on beamline X3B at the National
Synchrotron Light Source, which is supported by the U.S.
Department of Energy and the National Institutes of
Health. We also thank M. Costas and A. Ghosh for
valuable suggestions.
Supporting Online Material
www.sciencemag.org/cgi/content/full/1133417/DC1
Materials and Methods
SOM Text
Figs. S1 to S3
Tables S1 to S6
References
3 August 2006; accepted 12 December 2006
Published online 21 December 2006;
10.1126/science.1133417
Include this information when citing this paper.
include direct routes, such as aggregation and
incorporation into settling detritus, and indirect
export through the consumption of picoplankton
aggregates by organisms at higher trophic levels.
The network analysis used in these studies (4)
estimates the total particulate organic carbon
(POC) flux that originated from each input
source, here the NPP of each phytoplankton size
class. In the EqPac, for example, picoplankton
contributed 70% or more of the total NPP measured during JGOFS EqPac time series cruises
and were responsible for 87% of POC export via
detritus and 76% of carbon exported through the
mesozooplankton (5). Mesozooplankton consumed both picoplankton-derived detritus and
picoplankton-fed micrograzers. Similarly, at a
northern station in the Arabian Sea during the
Northeast Monsoon, picoplankton NPP was 86%
of the total and was the source for 97 and 75% of
the total carbon exported from the euphotic zone
via the POC and mesozooplankton pathways,
respectively (6). The relative contributions of the
picoplankton to carbon export decreased where
they produced relatively less of the total NPP but
were nonetheless substantial (Fig. 1 and Table 1).
We believe that the contributions of picoplankton to carbon flux from oceanic surface
layers have been overlooked because of assumptions that are made about cell size, sinking
dynamics, and the trophic pathways of picoplankton through ecosystems. The seminal paper
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The inclusion of small phytoplankton in
marine snow aggregates is well documented
(2, 17–19). Aggregates of intact Emiliania
huxleyi were first found in sediment traps deployed for short time periods (24 to 48 hours) in
the North Sea (20). In the northeast Atlantic, water
samples captured with bottles showed concentrations of Synechococcus-like cyanobacteria
on aggregates that were 3000 to 12,000 times
higher in concentration than that seen in freeliving forms (18). Picoplankton aggregates have
also been observed in sediment traps equipped
with acrylamide gels during short-term (48 hours)
deployments in high-nutrient, low-chlorophyll
waters off New Zealand (19). It is noteworthy that
observations of aggregates of small phytoplankton
in sediment traps have been in traps deployed for
short time periods, which will minimize loss of
material and maximize potential identification of
constituent organisms as compared to longer-term
deployments (21).
Although we did not explicitly include the
process of aggregation in our EqPac and Arabian
Sea analyses, we did allow ungrazed picoplankton
production to flow directly to the detritus pool,
where it could settle out as detritus or be consumed
by larger zooplankton. Models of food webs and
biogeochemical cycling (22–25) generally assume
that all picoplankton production is cycled through
the microbial loop and that none sinks from the
euphotic zone directly. This follows the classic
analysis of pelagic community structure and
nitrogen fluxes by Michaels and Silver (1), who
assumed that “only large particles, with consequently high potential sinking rates, can exit the
euphotic zone” and that “large colonies of smaller
algae” decompose (and are presumably recycled)
within the euphotic zone. Implicit in these food
web structures is the assumption that growth and
grazing in picoplankton-dominated open oceans
are in balance over long (annual) time scales (26).
However, our studies (5, 6) and those of others (27)
have shown that microzooplankton grazing does
not always balance picoplankton growth on
shorter time scales (weeks to months). Food
web models that force all picoplankton production through the microbial loop and do not allow
direct picoplankton export may, therefore, be
misleading. The conclusion of Michaels and Silver
(1) that “picoplankton, the dominant producers
in the model, contribute little to the sinking
material” was based on a model (theirs) that was
Downloaded from www.sciencemag.org on March 2, 2007
by Smayda (7) documented the tendency of
larger cells to sink faster. However, there are at
least three potential mechanisms for increasing
the effective size of picoplankton and their removal rates from the euphotic zone. First, the
aggregation of picoplankton cells into larger
detrital particles (8, 9) enhances their vertical
settling velocities and resulting export fluxes
(10–12). A simple model of aggregation and cell
sinking for phytoplankton of varying diameters
(3) (Fig. 2) shows that, at peak velocities, the
average settling rate for aggregated cells from
1 to 30 mm in diameter is similar, although aggregation does not substantially increase the settling
rates of the largest cells modeled (100 mm). We
conclude that an individual alga does not need to
be large to sediment out, even though settling
rates are generally faster for single cells that are
larger. Aggregation may be enhanced if cells are
nutrient-depleted (13), and settling may be
enhanced by the incorporation of mineral matter
(14–16).
Table 1. Direct and indirect contributions of picoplankton to carbon export from the euphotic zone for
two cruises in the EqPac and at three stations (N7, S2, and S11) during three seasons in the Arabian Sea.
Abbreviations are as follows: TS1, time series 1 (March to April 1992); TS2 Early, time series 2 cruise
(early October 1992); TS2 Mid, midway through TS2 (mid-October 1992); TS2 Late, late October 1992;
NEM, Northeast Monsoon; SIM, Spring Intermonsoon; and SWM, Southwest Monsoon.
Model
Export pathway
TS1
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
Carbon export due
to picoplankton
(mmol of C m−2 day−1)
% Contribution of
picoplankton to total
carbon export flux
EqPac
TS2 Early
TS2 Mid
TS2 Late
NEM N7
NEM S2
NEM S11
SIM N7
SIM S2
Fig. 1. Proportional contributions of varying phytoplankton groups or size classes (picoplankton,
diatoms, pelagophytes, and prymnesiophytes for
the EqPac study and pico-, nano-, and microphytoplankton for the Arabian Sea) to NPP versus their
proportional contributions to export as detritus (A) or
through consumption of mesozooplankton (B). Proportional contributions were calculated as NPP or
export due to the size class/total NPP or export flux.
SIM S11
SWM N7
SWM S2
SWM S11
www.sciencemag.org
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
POC
Mesozooplankton
SCIENCE
VOL 315
1.7
10.4
0.7
11.5
1.5
11.0
1.7
11.2
Arabian Sea
1.0
11.5
3.8
5.0
4.3
11.1
3.7
3.4
5.9
2.4
2.8
11.0
2.3
1.7
13.8
1.4
10.5
0.8
9 FEBRUARY 2007
87
76
57
60
43
50
63
63
97
75
56
33
99
83
73
24
92
89
98
80
91
68
53
34
44
1
839
Average velocity (m d – 1 )
14
Fig. 2. Average sinking velocity
100 μm
versus time (in days) for phytoplankton cells with diameters of 1,
12
3, 10, 30, and 100 mm. A cell density was assigned that is consistent
10
with the velocity versus cell diameter
30 μm
graph of Smayda (7) for 3-, 10-, 30-,
8
10 μm
and 100-mm cells. Because 1-mm
3 μm
cells are outside the range analyzed
6
by Smayda, a density difference of
0.0725 g cm−3, characteristic of
1 μm
4
Synechococcus lividus, was used
(3). Cells grow exponentially in a
2
mixed layer of constant thickness,
and there was no light or nutrient
limitation. Algal cells collide to form
0
8
10
12
14
16
18
20
22
24
aggregates at rates that depend on
Time (d)
their abundances as well as sizes.
Large cells settle faster than small ones. With time, cell concentrations increase, causing an increase in the
fraction of material in aggregates. The resulting increase in average particle size leads to an increase in
average settling speed. Peaks in total cell concentration occur when the enhanced losses due to settling
balance the gains due to cell division. The maximum average settling rate for particles formed from the 1-mm
cells is not substantially different from that for particles formed from the 30-mm cells.
structured in such a way that no other conclusion could be reached.
A second pathway for the accelerated sinking of
picoplankton-derived material is through mesozooplankton grazing. Picoplankton are usually considered to be too small to be captured effectively by
larger grazers such as copepods (28), but the
increase in effective size through aggregation makes
them available and thus can enhance their export
from surface layers through their incorporation into
fast-sinking fecal pellets (9). When mesozooplankton consume picoplankton-containing aggregates,
the picoplankton carbon short-circuits the microbial loop and results in higher than expected efficiency of carbon transfer from the euphotic zone
(18, 29, 30). For animals such as salps that are
capable of feeding on particles as small as 1 mm,
aggregation is unnecessary to produce fecal pellets.
The aggregates described in (19) were thought to
originate in salp or other tunicate fecal material.
The incorporation of picoplankton-sized particles
into the rapidly sinking mucous nets and feces of
filter feeders such as salps or pteropods provides an
additional route for picoplankton removal (2, 31).
We propose, therefore, that the conventional
view of carbon cycling, in which picoplankton
carbon is recycled within the microbial loop and
only larger phytoplankton carbon is exported,
should be revised to include the alternative
pathways for picoplankton carbon cycling discussed above. This alternative view relies on aggregation as a mechanism for both direct sinking
(the export of picoplankton as POC) and
mesozooplankton- or large filter feeder–mediated
sinking of picoplankton-based production, but
we believe that the evidence for both these processes under an array of environmental conditions is well established. Despite their small
size, picoplankton may contribute more to oceanic carbon export than is currently recognized, and
these contributions should be considered in current models of trophic dynamics in the ocean.
840
References and Notes
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2. L. Legendre, J. Le Fèvre, Aquat. Microb. Ecol. 9, 69 (1995).
3. Materials and methods are available as supporting
material on Science Online.
4. R. E. Ulanowicz, NETWRK4: A Package of Computer
Algorithms to Analyze Ecological Flow Networks
(Chesapeake Biological Laboratory, Univ. of Maryland,
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M. R. Roman, Deep-Sea Res. I 51, 1245 (2004).
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M. R. Roman, Deep-Sea Res. II 53, 555 (2006).
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This work was supported by NSF (grants OCE 0097296
and OCE 0352127 to G.A.J.).
Supporting Online Material
www.sciencemag.org/cgi/content/full/315/5813/838/DC1
Materials and Methods
References
4 August 2006; accepted 20 December 2006
10.1126/science.1133471
Integration of TGF-b and
Ras/MAPK Signaling Through
p53 Phosphorylation
Michelangelo Cordenonsi, Marco Montagner, Maddalena Adorno, Luca Zacchigna,
Graziano Martello, Anant Mamidi, Sandra Soligo, Sirio Dupont, Stefano Piccolo*
During development and tissue homeostasis, cells must integrate different signals. We investigated
how cell behavior is controlled by the combined activity of transforming growth factor–b
(TGF-b) and receptor tyrosine kinase (RTK) signaling, whose integration mechanism is unknown.
We find that RTK/Ras/MAPK (mitogen-activated protein kinase) activity induces p53 N-terminal
phosphorylation, enabling the interaction of p53 with the TGF-b–activated Smads. This mechanism
confines mesoderm specification in Xenopus embryos and promotes TGF-b cytostasis in human
cells. These data indicate a mechanism to allow extracellular cues to specify the TGF-b geneexpression program.
ross-talk between signaling pathways is
necessary to effect efficient and fine-tuned
regulatory control over metazoan development and physiology. TGF-b and receptor
tyrosine kinase (RTK) ligands are pleiotropic
cytokines affecting several aspects of cell behav-
C
9 FEBRUARY 2007
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ior, ranging from differentiation and proliferation to movement and survival (1, 2). Previous
work has shown that these signaling pathways
are integrated: The Ras/MAPK cascade, which
is downstream of RTK signaling, affects TGFb–induced mesoderm development in vertebrate
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