Deep-Sea Research II 53 (2006) 1573–1592
Photosynthetic electron turnover in the tropical and subtropical
Atlantic Ocean
David J. Suggett
a,
, C. Mark Moore
a,b
, Emilio Maran
˜
o
´
n
c,1
, Claudia Omachi
d
,
Ramiro A. Varela
e
, Jim Aiken
f
, Patrick M. Holligan
b
a
Department of Biological Sciences, University of Essex, Colchester, CO4 3SQ, UK
b
National Oceanography Centre, European Way, Empress Dock, Southampton, SO14 3ZH, UK
c
Departamento de Ecologı
´
a y Biologı
´
a Animal, Universidad de Vigo, 36200 Vigo, Spain
d
CTTMar/UNIVALI, Rua Uruguai, 458 Itajaı
´
, 88302-202, Brazil
e
Universidad de Vigo, Campus Lagoas-Marcosende, 36200 Vigo, Spain
f
Plymouth Marine Laboratory, Prospect Place, Plymouth, PL1 3DH, UK
Received 31 August 2005; received in revised form 20 January 2006; accepted 14 May 2006
Available online 4 August 2006
Abstract
Photosynthetic electron transport directly generates the energy required for carbon fixation and thus underlies the
aerobic metabolism of aquatic systems. We determined photosynthetic electron turnover rates, ETRs, from ca. 100 FRR
fluorescence water-column profiles throughout the subtropical and tropical Atlantic during six Atlantic Meridional
Transect cruises (AMT 6, May–June 1998, to AMT 11, September–October 2000). Each FRR fluorescence profile yielded
a water-column ETR-light response from which the maximum electron turnover rate ðETR
max
RCII
Þ, effective absorption
(s
PSII
) and light saturation parameter (E
k
) specific to the concentration of photosystem II reaction centres (RCIIs) were
calculated. ETR
max
RCII
and E
k
increased whilst s
PSII
decreased with mixed-layer depth and the daily integrated
photosynthetically active photon flux when all provinces were considered together. These trends suggested that variability
in maximum ETR can be partly attributed to changes in effective absorption. Independent bio-optical measurements taken
during AMT 11 demonstrated that s
PSII
variability reflects taxonomic and physiological differences in the phytoplankton
communities. ETR
max
RCII
and E
k
, but not s
PSII
, remained correlated with mixed-layer depth and daily integrated
photosynthetically active photon flux when data from each oceanic province were considered separately, indicating a
decoupling of electron turnover and carbon fixation rates within each province. Comparison of maximum ETRs with
14
C-based measurements of P
max
further suggests that light absorption and C fixation are coupled to differing extents for
the various oligotrophic Atlantic provinces. We explore the importance of quantifying RCII concentration for
determination of ETRs and interpretation of ETR-C fixation coupling.
r 2006 Elsevier Ltd. All rights reserved.
Keywords: AMT; Subtropical gyres; Tropical equatorial; Phytoplankton; Fast Repetition Rate fluorometry; Photosynthetic electron
turnover
ARTICLE IN PRESS
www.elsevier.com/locate/dsr2
0967-0645/$ - see front matter r 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2006.05.014
Corresponding author.
E-mail address: dsuggett@essex.ac.uk (D.J. Suggett).
1
Present address: Laboratoire d’Oce
´
anographie de Villefranche, CNRS—UPMC, 06234 Villefranche-sur-Mer, France.
1. Introduction
Routine oceanographic measurements of primary
productivity trace the evolution of O
2
or assimila-
tion of inorganic carbon (C
i
) or nitro gen. Flu xes of
these elements between phytoplankton and their
surrounding environment indica te the net commu-
nity metabolism and thus the trophic structure of
the food web and significance of carbon sequestra-
tion (Karl et al., 1 998; Serret et al., 2001; Gonza
´
lez
et al., 2002). Furthermore, the light-response of
these productivity measurements describe the phy-
siological status of photoautrophic communities
that then can be applied to models investigating
environmental change (Sathyendranath et al., 1995;
Maran
˜
o
´
n and Holligan, 1999). Consequently, con-
siderable effort has been made in recent years to
characterise O
2
evolution and C
i
assimilation in the
large and vastly under-sampled oceanic tropical and
subtropical regions (Karl et al., 1998; Maran
˜
o
´
n
et al., 2000; Serret et al., 2001; Gonza
´
lez et al., 2002;
Maran
˜
o
´
n, 2005).
Autotrophic O
2
evolution and C
i
assimilation are
governed by the rate of electron turnover by the
photochemical ‘light’ reactions (Allen, 2002; Beh-
renfeld et al., 2004; Kramer et al., 2004). Absorbed
light energy promotes the splitting of water to
release O
2
, protons and electrons. Each electron is
transferred between a series of redox molec ules to
provide the reductant used to fix CO
2
into organic
matter. Electron transfer also results in the accu-
mulation of protons within the lumen of the
thylakoid membranes. A gradient of protons across
the thylakoid membranes drives synthesis of ATP
via ATP synthase. ATP is then used to fix C
i
but is
also consumed by additional energy-demanding
processes that are crucial for the maintenance and
regulation of photochemical pathways, in particular
uptake and assimilation of nutrients including C
i
(Falkowski and Raven, 1997; Allen, 2002; Kramer
et al., 2004). ATP also can be provided by
respiration (Badger et al., 2000; Geider and
MacIntyre, 2002) but at the expense of previously
fixed carbon. Therefore, characterising the varia-
bility of electron turnover rates can potentially
provide a more detailed understanding of the role of
primary productivity upon aquatic community
metabolism than simply tracing C
i
or O
2
.
Electron turnover rates (ETRs, linear e
turnover
per unit biomass per unit time) of microalgae can be
determined using chlorophyll a fluorescence induc-
tion techniques (Gorbunov et al., 2001; Kromkamp
and Forster, 2003; Suggett et al., 2003). One such
induction technique, Fast Repetition Rate (FRR)
fluorescence (Kolber et al., 1998), has become
widely used by oceanographers as it avoids the
need to incubate discr ete water samples and is
highly sensitive. However, despite these benefits,
relatively few FRR fluorescence-based measur e-
ments of marine primary productivity have been
reported (Suggett et al., 2001; Moore et al., 2003 ;
Raateoja et al., 2004; Smyth et al., 2004 ) and little is
known of the variability of ETRs in oligotrophic
subtropical and tropical oceanic environments.
Two main limitations account for the previous
sparsity of FRR-based information. Firstly, it has
been problematic to reconcile FRR determinations
of ETR with conventional O
2
evolution or C uptake
productivity measurements (Suggett et al., 2003;
Raateoja et al., 2004). ETRs are a direct measure of
the potential to split wate r and hence of O
2
production, provided that the maxi mum quantum
yield of O
2
evolution remains unchanged (Krom-
kamp and Forster, 2003). Two electron cycling
processes act to decouple ETR from net O
2
evolution, cycling of electrons around photosystem
II (PSII) and reduction of O
2
by the Mehler reaction
(Badger et al., 2000). Both PSII electron cycling
(Pra
´
s
ˇ
il et al., 1996) and the Mehler reaction (Kana,
1992; Lewitus and Kana, 1995) occur under
exposure to intense light. In addition, the Mehler
reaction is particularly pronounced in cyanophytes
(Kana, 1992; Lewitus and Kana, 1995). As such,
derivations of net O
2
from FRR-based ETRs may
be particularly problematic in the intense light,
cyanobacterial-dominated communities that are
typical of many subtropical and tropical marine
environments. Secondly, direct FRR-based mea-
surements alone are not enough to accurately
quantify volume-specific photoautotroph ic produc-
tivity rates since they are weighted to the excitation
wavelength that is employed and to the number of
functional photosystem II (PSII) reaction centres
(RCII) (Suggett et al., 2001, 2003). FRR-based
calculations of productivity that are wei ghted to the
RCII concentration are not problematic per se.
However, without specific knowledge of the RCII
concentration, such calculations are incomparable
with ‘conventional’ productivity measurements that
are typically weighted on a per unit algal pigment,
per cell or per unit volume of seawater basis.
In addition to O
2
evolution, photosynthetic linear
electron turnover drives protonation of the thyla-
koid lumen that is then available for ATP synthesis.
ARTICLE IN PRESS
D.J. Suggett et al. / Deep-Sea Research II 53 (2006) 1573–15921574
Therefore, we can re-define FRR-based ‘productiv-
ity’ more accurately as the energetic potential
available for all photosynthetic pathways. Also,
we can correct for the spectral weighting of FRR-
excitation (Babin et al., 1996; Suggett et al., 2001;
Raateoja et al., 2004) and obtain some knowledge
of the RCII concentration indirectly (Suggett et al.,
2001, 2004; Moore et al., 2005) provided additional
bio-optical and/or biophysical properties of the
PSII antenna-reaction centre complex are measured.
Here we employed FRR fluorometry to determine
the RCII normalised rate of electron turnover
(ETR
RCII
), and hence energetic potential for photo-
synthesis, by phytoplankton communities through-
out the subtropical and tropical Atlantic Ocean.
Water-column profiles of FRR fluorescence and
ETR
RCII
were used to derive maximum rates of
effective absorption, s
PSII
(max), and photosyn-
thetic electron turnover, ETR
max
RCII
, from six (ca. 100
casts) Atlantic Meridional Transects. Considerable
variability of both s
PSII
(max) and ETR
max
RCII
was
observed between and within subtropical and
tropical provinces throughout the sampling period.
We discuss the underlying mechanisms that may
account for this variability. Also, we consider the
importance of quantifying RCII concentrations for
determining chlorophyll- or volume-normalised
ETRs and for interpreting the coupling be tween
electron turnover and carbon fixation for these
subtropical and tropical provinces.
2. Methods
2.1. Sampling and instrument deployment
Data were collected during Atlantic Meridional
Transect (AMT) cruises 7–11 between Grimsby
(UK) and Montevideo (Uruguay), September
1998–October 2000 (Table 1, Fig. 1). Cruise
transects 7, 9 and 10 followed a similar track
between northern and southern subtropical gyres
via the western tropical Atlantic. In contrast,
transects 8 and 11 followed a route between
northern and southern subtropical gyres via Ascen-
sion Island and hence through the eastern tropical
Atlantic. Some data from AMT6 between Cape
Town (South Africa) and Grimsby (UK), May–
June 1998, are also included. Data from all six
cruises were separated into four Atlantic biogeo-
graphical provinces (Table 1): the northern sub-
tropical gyre-east (NSTG, 22–401N), the northern
tropical (NT, 6–221N), the eastern and western
tropical (ET, 161S–061N, 201W–201E; WT,
161S–061N, 20–601W), and the southern subtropical
gyre (SSTG, 16–35 1S).
A Seabird 911+ CTD-Niskin rosette system
and Plymouth Marine Laboratory-designed optical
rig were each deployed at least once per day and
to depths of 200–250 m. A Chelsea Instruments
FAST
tracka
FRR fluorometer with integrated
2p photosynthetically available radiation (PAR,
ARTICLE IN PRESS
Table 1
Number of FRR fluorescence casts with sampling dates and locations for Atlantic Meridional Transects (AMTs) 6–11
AMT Cruise 6 8 10 7 9 11
Sample dates
(FRRF)
14th May–12th
June 1998
3rd May–31st
May 1999
15th April–2nd
May 2000
16th Sept–14th
Oct 1998
22nd Sept–12th
Oct 1999
15th Sept–9th
Oct 2000
Sample seasons Austral autumn, Boreal spring Austral spring, Boreal autumn
NSTG (22–401N;
15–251W)
244544
NT (6–221N;
15–251W)
342443
ET (161S–061N;
201W–101E)
74 7
WT (161S–061N;
20–501W)
443
SSTG (16–351S;
20–501W)
74367
BENG (16–351S;
10–201E)
9
Cruises are separated into ‘northbound’ (6, 8 and 10) and ‘southbound’ (7, 9 and 11). Open ocean tropical and subtropical provinces are
modified from Longhurst et al. (1995), NSTG (north Atlantic subtropical gyre-east), NT (northern tropical Atlantic), ET (eastern Tropical
Atlantic), WT (western tropical Atlantic) and SSTG (south Atlantic subtropical gyre). The BENG (Benguela coastal upwelling) was also
sampled during AMT 6 but is not included in the data analyses here.
D.J. Suggett et al. / Deep-Sea Research II 53 (2006) 1573–1592 1575
400–700 nm irradiance) and pressure sensors was
fastened to the frame of the CTD-rosette during
AMTs 6–10 or integrated with the optical rig during
AMT 11. Both the FRR fluorometer and PAR
sensor were attached in such a way as to avoid
shadowing from other instruments. These instru-
ment packages were then deployed at approximately
local noon time from the sunward side of the ship.
Depths for collection of water samples using Niskin
bottles wer e determined from the downward tem-
perature and salinity profiles. Incident PAR was
measured continuously and integrated to give the
along track daily integrated photosynthetically
active photon flux density (PPFD).
Additional daily pre-dawn CTD casts also were
preformed throu ghout AMT 11. Simultaneous
optical and FRR fluorescence profiles were not
made. Instead, discrete water samples were imme-
diately drawn from the rosette and passed through
the enclosed chamber of the FRR fluorometer and
thus yielded discrete dark-adapted fluorescence
measurements.
2.2. Light absorption, pigments and optics
Bio-optical measurements were made from water
collected from the local noon casts during AMT 11
only. 1.5–3 L were filtered through 25 mm Whatman
GF/F filters and stored at 80 1C for onboard
measurements of particulate light absorption or
within liquid N
2
for HPLC analysis of phytoplank-
ton pigments upon return. Total particulate matter
absorption spectra were measured on the GF/F
filters mounted on an opal glass support using a
single beam Beckman DU650 scanning (l, 1-nm
intervals between 350 and 750 nm) spectrophot-
ometer. A separate GF/F was soaked in filtered
seawater and used as a blank. Phytoplankton
absorption on the filters, a (l)(m
1
), was deter-
mined as described previously (Suggett et al., 2001),
aðlÞ¼
2:303ODðlÞS
bðlÞV
, (1)
where OD (l) is the optical density of all particulate
material retained on the filter minus that at 750 nm,
V is the volume of filtered seawater (m
3
), and S is
the particulate retention area of the GF/F filter
measured using the spectrophotometer (m
2
). b (l)is
the pathlength amplification factor and was esti-
mated as
bðlÞ¼1:63ODðlÞ
0:22
. (2)
Contribution of light absorption by particulate
detritus a
d
(l) upon a (l) was determined num eri-
cally following the method of Bricaud and Stramski
(1990) improved for low detritus content (Varela
et al., 1998).
Concentrations of both ‘photosynthetically ac-
tive’ (PS, mono- and di-vinyl chlorophylls a and b,
chlorophyll c, Peridinin, fucoxanthin, 19
0
-hexanoy-
loxyfucoxanthin, 19
0
-butanoyloxyfucoxanthin and
prasinoxanthin) and ‘non-photosynthetically ac-
tive’, or ‘photoprotective’ (PP, violaxanthin, diadi-
noxanthin, alloxanthin, lutein, zeaxanthin and
b-carotene) pigments were determined using a Thermo
Separations product HPLC as described previously
(Barlow et al., 2002).
Underwater optical spectra at depths correspond-
ing with particulate absorption and pigment sam-
ples were determined from irradiance and radiance
measured at seven wavelengths (412, 443, 490, 510,
555, 620 and 670 nm) (Satlantic multispectral
optical sensors, Satlantic Inc., Canada). To obtain
spectrally resolved in situ light between 400 and
700 nm, in situ wavelengths were interpolated non-
linearly following the shape of a global climatolo-
gical spectrum as described previously (Suggett
et al., 2001).
ARTICLE IN PRESS
Fig. 1. Sampling locations of Fast Repetition Rate (FRR)
fluorescence casts in the tropical and subtropical Atlantic during
AMTs 6–11.
D.J. Suggett et al. / Deep-Sea Research II 53 (2006) 1573–15921576
2.3. FRR fluorescence and determination of electron
transport rates
Throughout all cruis es, the FRR fluorometer was
programmed to deliver and record single photo-
chemical turnover excitation and emission se-
quences as described by Moore et al. (2003, 2005)
and Suggett et al. (2003, 2004). Specifically,
saturating-chain sequences of 100 1.1 ms flashes
were applied at 2.8 ms intervals. Fluorescence
transients were logged internally during profiling
from the average of 16 of these sequences delivered
in succession. This data acquisition protocol was
then alternated between the ‘open’ and ‘enclosed’
FRR chambers at an interval of 30 ms. The gain was
set prior to deployment according to that employed
by a second FAST
tracka
FRR fluorometer on ‘auto-
gain’ plumbed into the underway non-toxic surface
seawater supply. Any data that exhibited saturation
of the FRR photomultiplier tube were excluded
from further analyses. Discrete samples from the
pre-dawn casts during AMT 11 were held in the
‘enclosed’ chamber and exposed to 50 individual
sequences each separated by 1-s intervals. These 50
acquisitions were logged internally and subse-
quently averaged into a single, high signal: noise
transient (see Suggett et al., 2004). Similarly, all
logged fluorescence transients from each vertical
cast per station were averaged into 5–10 m depth
bins to increase the signal to noise ratio. Fluores-
cence transients were finally fitted to the biophysical
model of Kolber et al. (1998) using ‘v4’ software
(Laney, 2003) to yield values of minimum and
maximum fluorescence (F
min
, F
max
) and the effective
absorption cross sectio n (s
PSII
).
Obtaining accurate absolute values of biophysical
parameters from the fluorescence transients requires
the subtraction of both inst rument response func-
tion (IRF) non-linearities (Laney, 2003) and,
depending on the parameter, sample blanks (Cullen
and Davis, 2003). An IRF was only determined
following the final cruise, AMT 11 using a
chlorophyll a extract and deionised water (Laney,
2003; Suggett et al., 2004; Moore et al., 2005) for all
gains and both FRR chambers. We subsequently
applied this IRF to fluorescence transients obtained
from all prior cruises. Sample blanks were not taken
throughout AMTs 6–11. Instead, we used an
approach for calculating electron transport rates
ETR that is independent of the need for sample
blanks. Our approach is based on that of Gorbunov
et al. (2001) and uses only two parameters easily
obtained from FRR fluorometry in situ under
actinic light, the PSII effective absorption cross
section, s
PSII
0
(A
˚
2
quanta
1
), and PSII trapping
efficiency of excitons (F
q
0
/F
v
0
, dimensionless), in
addition to the PPFD,
ETR
RCII
¼ PPFDs
PSII
0
F
0
q
=F
0
v
0:006023, (3)
where ETR
RCII
is the rate of electron turnover
normalised to the number of PSII reaction centres
(mol e
mol RCII
1
s
1
) and 0.006023 is a factor
that accounts for the conversion of s
PSII
0
from A
˚
2
quanta
1
to m
2
mol RCII
1
and of PPFD from
mmol photons m
2
s
1
to mol photons m
2
s
1
.
Here, F
q
0
/F
v
0
is estimated as the ratio of (F
max
F
min
)/F
min
from the ‘open’ and ‘enclosed’ chambers,
F
0
q
=F
0
v
¼
ðF
max
F
min
Þ=ðF
max
f Þ
OPEN chamber
ðF
max
F
min
Þ=ðF
max
f Þ
ENCLOSED chamber
.
(4)
The proportion of ‘‘non-active’’ fluorescence (f,the
sample blank) inherent to fluorescence yield mea-
surements cancel in Eq. (4). However, this calcula-
tion of F
q
0
/F
v
0
makes two assumptions: (1) the two
FRR chambers are directly comparable and (2) that
the brief period of time within the FRR enclosed
chamber allows for total Q
A
reoxidation. We have
confidence that the first assumption was met since the
two chambers yielded the same fluorescence yields at
depths where non-photochemical quenching was
absent (data not shown). However, the second
assumption may not always be met because slow
Q
A
reoxidation may occur without supplementary
far red light, which is not provided by the FAST
tracka
FRR fluorometer.
Direct in situ FRR measurements of s
PSII
0
are
weighted to the LED spectrum of the FRR
fluorometer (termed s
PSII
0
,478
, Moore et al., 2006,
and references therein). Accurate application of
Eq. (3) in situ requires that s
PSII
0
,478
be adjusted to
the spectrum of light that phytoplankton receive in
situ, s
PSII
0
,in situ
. Therefore, effective absorption
coefficients,
¯
a (m
1
), were determined from spectrally
resolved particulate absorption, a (m
1
), and excita-
tion by the FRR fluorometer LEDs or by the light
field in situ (PPFD (l), mmol m
2
s
1
nm
1
),
¯
aðlÞðzÞ
¼
X
700
400
aðlÞðzÞPPFDðlÞðzÞ
.
X
700
400
PPFDðlÞðzÞ
ð5Þ
ARTICLE IN PRESS
D.J. Suggett et al. / Deep-Sea Research II 53 (2006) 1573–1592 1577
