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The fate of photons absorbed by phytoplankton in the global ocean

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Using solar energy suboptimally How efficient are phytoplankton at converting sunlight into the products of photosynthesis? The two other pathways that that absorbed energy can take are emission back to the environment by fluorescence or conversion to heat. Lin et al. measured phytoplankton fluorescence lifetimes in the laboratory and combined them with satellite measurements of variable chlorophyll fluorescence. Combined, they determined the quantum yields of photochemistry and fluorescence in four ocean basins. Approximately 60% of absorbed solar energy is converted to heat, a figure 50% higher than has been determined for conditions of optimal growth. Science , this issue p. 264
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REPORTS
Cite as: H. Lin et al., Science
10.1126/science.aab2213 (2016).
For several decades, chlorophyll concentrations based on
remotely sensed variations in ocean color have been used to
derive global phytoplankton productivity (1, 2). Primary
productivity models implicitly include physiological
processes, but their explicit representation has, thus far,
been elusive (3, 4). Variable chlorophyll fluorescence is the
most sensitive, non-destructive signal detectable in the
upper ocean that reflects instantaneous phytoplankton
photophysiology (57). Over the past two decades, many
hundreds of thousands of discrete in situ measurements of
variable fluorescence have been made using ship-based
active fluorometers. These instruments, primarily designed
to quantify the quantum yield of photochemistry (Fv/Fm) in
photosystem II (PSII), the reaction center responsible for
splitting water, have been used to follow phytoplankton
photophysiology in response to iron fertilization (8), across
eddies (9, 10) along meridional transects (11), and many
other phenomena (12, 13). Although active variable
fluorescence measurements have become almost routine, by
themselves, they do not allow closure on the fate of light
absorbed by phytoplankton. Here, we report the fraction of
sunlight absorbed by phytoplankton that actually is used to
form chemical bonds in the global ocean. Further, we
compare the spatial distributions of photochemical energy
conversion to the pattern inferred from space-based
retrievals of solar induced fluorescence yields
The biophysical basis of fluorescence measurements de-
rives from the three possible fates of solar energy absorbed
by any photosynthetic organism (14). Absorbed photons can
(1) generate photochemical reactions leading to production
of organic matter (with the rate kp), (2) be dissipated as heat
(kt), or (3) be emitted back to the environment as fluores-
cence (kf) (15). In a dark-adapted state or under low irradi-
ance (when kt is constant), the quantum yield of chlorophyll
fluorescence, ϕf (= kf/(kp+kt+kf)), is inversely related to the
quantum yield of photochemistry in PSII, ϕp = kp/(kp+kt+kf)
= Fv/Fm.
Substitution and rearrangement leads to:
ϕf = ϕfm (1 – Fv/Fm) (1)
where ϕfm (= kf/(kt+kf)) is the maximum fluorescence yield
obtained when photochemistry is nil (e.g., at saturating
background light).
This biophysical model predicts an inverse linear rela-
tionship between the quantum yield of photochemistry and
that of chlorophyll fluorescence. However, by the early
1980’s it was realized that exposure to high continuous irra-
diance can lead to a suite of thermal dissipative mecha-
nisms, collectively called non-photochemical quenching
(NPQ) (16). These reactions markedly decrease the quantum
yield of fluorescence at high background light. Hence, the
relationship between chlorophyll fluorescence and photo-
chemistry, described in Eq. 1, becomes highly non-linear as
NPQ phenomena play an increasingly larger role in energy
dissipation.
Calculating the budget of absorbed solar radiation re-
quires measurements of the quantum yields of at least two
pathways, for example, photochemistry and fluorescence.
Although the development and use of variable fluorescence
techniques over the past two decades has provided unprec-
The fate of photons absorbed by phytoplankton in the
global ocean
Hanzhi Lin,1* Fedor I. Kuzminov,1 Jisoo Park,2 SangHoon Lee,2 Paul G. Falkowski,1,3† Maxim Y. Gorbunov1†
1Environmental Biophysics and Molecular Ecology Program, Department of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New
Brunswick, NJ, USA. 2Korea Polar Research Institute, 26 Songdomirae-ro, Yeonsu-Gu, Incheon, Republic of Korea. 3Department of Earth and Planetary Sciences, Rutgers,
The State University of New Jersey, Piscataway, NJ, USA.
*Present Address: Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Sciences, Baltimore, MD 21202, USA.
†Corresponding author. E-mail: falko@marine.rutgers.edu (P.G.F.); gorbunov@marine.rutgers.edu (M.Y.G.)
Solar radiation absorbed by marine phytoplankton can follow three possible paths. By simultaneously
measuring the quantum yields of photochemistry and chlorophyll fluorescence
in situ,
we calculate that,
on average, ~60% of absorbed photons are converted to heat, while only 35% are directed toward
photochemical water splitting and the rest are re-emitted as fluorescence. The spatial pattern of
fluorescence yields and lifetimes strongly suggests that photochemical energy conversion is
physiologically limited by nutrients. Comparison of in situ fluorescence lifetimes with satellite retrievals
of solar induced fluorescence yields suggest that the mean values of the latter are generally
representative of the photophysiological state of phytoplankton, however the signal to noise ratio is
unacceptably low in extremely oligotrophic regions, which comprise 30% of the open ocean
First release: 7 January 2016 www.sciencemag.org (Page numbers not final at time of first release) 1
edented information about photochemical conversion in
phytoplankton in situ, these instruments are unable to
measure the absolute quantum yields of fluorescence. To
overcome this basic limitation, we constructed an extremely
sensitive sea-going instrument that measures chlorophyll
fluorescence lifetimes in the picosecond time domain (17).
The fluorescence lifetime can be quantitatively related to
the absolute quantum yield of fluorescence (18):
ϕf = τ/τn (2)
where τn is the intrinsic (or natural) lifetime constant for
chlorophyll a molecules (17). Thus, the longer the lifetime,
the higher the quantum yield of fluorescence.
Between 2008 and 2014, we obtained >150,000 discrete
chlorophyll fluorescence lifetime measurements from the
Pacific, Atlantic, Arctic, and Southern Oceans. These meas-
urements comprise the map of quantum yields of chloro-
phyll fluorescence from phytoplankton in the upper ocean
(Fig. 1). The night-time in situ lifetimes ranged from 0.5 to
2.7 ns with a mean of 1.13 ± 0.33 ns (Fig. 2). This naturally
dark-adapted condition corresponds to a state when all
functional reaction centers are open and NPQ is absent.
These values span the entire range of published lifetimes of
in vivo chlorophyll fluorescence obtained from cultured
phytoplankton (17) and reflect extraordinary variability in
phytoplankton physiology in the global ocean. The general
pattern of the fluorescence lifetimes in the central gyres of
the global ocean is rather featureless although phytoplank-
ton growth is subject to both macro- and micronutrient lim-
itation (14). The shortest fluorescence lifetimes (<1ns) were
observed along continental margins, in the Antarctic con-
vergence, Subtropical Atlantic and Pacific oceans. These
lifetime distributions support the hypothesis that phyto-
plankton in the central gyres are acclimated to broad scale
and persistent nutrient limitation (11, 12). In contrast the
longest fluorescence lifetimes were observed in high-
nutrient-low-chlorophyll (HNLC) regions of the equatorial
Pacific Ocean and the Southern Ocean where primary pro-
duction is limited by the paucity of iron (19), a micronutri-
ent that is critical for the function of photosystem II (20,
21). The exceptionally high values of fluorescence lifetimes
in these areas of the global ocean are consistent with ex-
tremely low Fv/Fm values and indicative of a large fraction of
non-functional PSII reaction centers and energetically un-
coupled antenna pigment-protein complexes (2123).
There is a strong diel cycle in fluorescence lifetimes; in
general, lifetimes were longer at night than during daytime,
in spite of a marked reduction in the quantum yields of
photochemistry under strong sunlight (Fig. 2). The >5 fold
variability in dark-adapted fluorescence lifetimes in situ far
exceeds that predicted by Eq. 1. However, this dynamic
range is greatly attenuated in high light, when NPQ pro-
cesses are activated. For example, exceptionally long life-
times (>2 ns) measured in a dark-adapted state in HNLC
regions decrease by more than two-fold in high light,
whereas relatively short lifetimes (~ 1 ns) in low-nutrient-
low-chlorophyll (LNLC) regions decrease by only 30% under
the same conditions (Fig. 2A). Regardless of the molecular
mechanisms responsible for NPQ, the net result for high
light conditions is increased thermal dissipation of absorbed
light in PSII leading to both reductions in photochemical
energy conversion efficiency and in the range of variability
of the quantum yields of fluorescence.
With the launch of the Moderate Resolution Imaging
Spectroradiometer (MODIS) and MEdium Resolution Imag-
ing Spectrometer (MERIS) satellites, which possess the ca-
pability of remotely detecting solar induced chlorophyll
fluorescence signals from the global ocean, it became theo-
retically possible to calculate the quantum yield of chloro-
phyll fluorescence from space (2426). However, the
theoretical basis for estimating the relationship between
chlorophyll fluorescence and photochemistry was developed
before there was an understanding of NPQ (24). We there-
fore examined how the measured in situ fluorescence life-
times are related to satellite-derived estimates of the
quantum yield of chlorophyll a fluorescence.
Statistical analyses (effective sample size >20,000) by
both Pearson’s linear correlation coefficient and two non-
parametric Kendall’s tau and Spearman’s rho coefficients
revealed a weak linear correlation (p<0.01) between these
satellite derived solar induced fluorescence yields and the
ship based measurements (Table S1). Satellite-based esti-
mates of the quantum yield are derived from observations of
the surface ocean close to local noon (27). Hence, the re-
motely sensed estimates inevitably are obtained at very high
irradiances and are strongly influenced by NPQ, a phenom-
enon that is extremely difficult to quantify in global bio-
physical models. NPQ is not only critically dependent on
pigment composition within the light harvesting antennae
(which, in turn, is affected by phytoplankton community
composition), but also on upper ocean turbulence as it af-
fects the light field experienced by the community (28), as
well as nutrient stress (19). Despite these complications,
qualitative comparison of satellite-derived maps of quantum
yields of chlorophyll fluorescence (Fig. 3) reveals basic
trends that often, but not always correspond to in situ life-
time measurements. For example, in the Southern Ocean
(an HNLC region), satellite-derived quantum yields are high
and correlate with long lifetimes. In this iron limited region
of the world oceans, there is a well-documented reduction in
photosynthetic energy conversion efficiency as a result of
impairment of PSII reaction centers and potential energetic
uncoupling of the antenna pigment-protein complexes (7,
22). In the low nutrient, low chlorophyll regions of the cen-
tral oceanic gyres of the North and South Pacific and the
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North Atlantic, measured fluorescence lifetimes are signifi-
cantly shorter compared to HNLC regions. Although the
mean fluorescence yield based on the satellite retrievals for
the oligotrophic open ocean is 0.043 (Fig. 4) and is generally
concordant with that measured in situ values, the high es-
timates of quantum yields obtained from the space-based
platform (Fig. 3) are not corroborated by in situ lifetime
measurements. Further, the range of estimated quantum
yields derived from satellite-based measurements (> six
fold) is far larger than that of the in situ lifetimes measured
at high irradiances (~ 3-fold). Indeed, the range of the esti-
mated quantum yields of fluorescence in the global ocean (~
0.02 to 0.15) appears to exceed that of our current biophysi-
cal understanding of photochemistry in phytoplankton.
What might be the source of this discrepancy?
In the central ocean gyres, where surface chlorophyll
concentrations are very low (<0.1 mg·m−3), the fluorescence
signals propagated to space are extremely weak. As a result,
the current algorithms used to calculate quantum yields of
fluorescence become increasingly uncertain (Fig. 4 and (26,
29)). The relationship between measured lifetimes and satel-
lite-derived quantum yields diverge. In contrast to the satel-
lite-derived yields which have significant “noise”, the in situ
lifetime measurements remain extremely precise (within
5%) even at the lowest chlorophyll concentrations found in
the upper ocean. Another factor behind this discrepancy is
the effect of pigment packaging within a phytoplankton cell
(25, 30, 31), which is most pronounced in larger cells and
reduces the observed quantum yields, as compared to their
true “molecular” values inferred from lifetime measure-
ments. Similarly, the uncertainties of the current algorithms
for remote sensing retrievals of phytoplankton absorption
coefficients (25) further reduce the accuracy of satellite-
based estimates of the quantum yields.
Although quantum yields of chlorophyll fluorescence ob-
tained from current satellite sensors have many inherent
inaccuracies, this approach to understanding global photo-
physiology of phytoplankton should not be abandoned. We
suggest that relating the space-based estimates to in situ
measurements of chlorophyll fluorescence lifetimes will
provide a pathway to understanding photobiological energy
utilization and dissipation processes on a global scale. For
example, the maximal average photochemical energy con-
version efficiency (ϕp) at night in the global ocean, obtained
simultaneously with our lifetime measurements, is 0.35 ±
0.11 (Fig. S2). Given an average night-time lifetime of 1.13 ns
(Fig. 2), we deduce that thermal energy dissipation accounts
for ~ 60% of the photosynthetically active quanta absorbed
by phytoplankton globally. In contrast, under optimal
growth conditions in the laboratory, an average phytoplank-
ton cell utilizes ~ 65% of the absorbed quanta for photo-
chemistry and dissipates <35% as heat. That thermal
dissipation of absorbed quanta by phytoplankton in the up-
per ocean is so high strongly implies that a large fraction of
cells have impaired or non-functional PSII reaction centers,
and/or uncoupled photosynthetic antenna. We conclude
that, while photochemical energy conversion to biomass in
the oceans accounts for half of the global carbon fixed per
annum, the overall energy conversion efficiency is relatively
low and is limited by nutrient supply
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ACKNOWLEDGMENTS
We thank Drs. E. Boyle, P. Quinn, K. Thamatrakoln, and V.Fadeev for providing
shiptime, and the captains and crews of RV Oceanus, RV Knorr, RV Melville, RV
Akademik Yoffe, and RV Araon. This research was supported by Grants
NNX08AC24G from NASA Ocean Biology and Biogeochemistry Program and SI-
1334 from the Strategic Environmental Research and Development Program to
MYG and PGF. HL and FIK were supported by the Institute of Marine and Coastal
Sciences post-doctoral fellowships and the Bennett L. Smith Endowment to PGF.
MYG and FIK were in part supported by Grant 14-17-00451 from the Russian
Science Foundation. JP and SL were supported by Grant PP15020 from the
Korean Polar Research Institute. All fluorescence data are deposited at
PANGAEA (Publishing Network for Geoscientific and Environmental Data) under
accession number PDI-11228.
First release: 7 January 2016 www.sciencemag.org (Page numbers not final at time of first release) 4
SUPPLEMENTARY MATERIALS
www.sciencemag.org/cgi/content/full/science.aab2213/DC1
Materials and Methods
Figs. S1 to S4
Table S1
References (3252)
30 March 2015; accepted 9 December 2015
Published online 7 January 2016
10.1126/science.aab2213
First release: 7 January 2016 www.sciencemag.org (Page numbers not final at time of first release) 5
chlorophyll fluorescence lifetimes
and the derived quantum yields of
fluorescence (Eq. 2) in the upper
nitrate concentrations in the world
ocean (32
sampling were (A) July-Aug. 2011;
(B) Oct.-Nov. 2011; (C) Oct.-Nov.
2010; (D) Jan. 2012; (E) July 2014;
(F) Sept. 2010; (G) May 2014; (H)
Aug. 2008.
Fig. 2. (A) Representative diel
cycles of chlorophyll fluorescence
lifeti
mes in HNLC and LNLC
regions of the Pacific Ocean
obtained in Oct. 2011. Color bar for
lifetimes is the same as in Fig. 1;
(
B
) Histograms of the fractional
frequency of lifetime
measurements in daytime and at
night, respectively. The mean value
of nighttime lifetimes is 1.13 ± 0.33
ns and that of daytime lifetimes is
1.02 ± 0.22 ns.
First release: 7 January 2016 www.sciencemag.org (Page numbers not final at time of first release) 6
Fig. 3. Global seasonal maps of quantum yields of solar induced chlorophyll
fluorescence in the upper ocean. (
A
) boreal winter (21 Dec. 2011 20 Mar., 2012); (
B
)
boreal spring (21 Mar. - 20 June, 2012); (
C
) boreal summer (21 Sept. 20 Dec., 2012);
(D) boreal autumn (21 Sept. 20 Dec., 2012).
Fig. 4. Variations in MODIS retrievals of the quantum yields of
chlorophyll fluorescence (N=5.17 ×106) with chlorophyll abundance (17).
The mean value of these satellite-derived quantum yields is 0.043. The
average value of in situ lifetime measurements at noon (between 10 a.m
to 2 p.m local time) is 0.99 ± 0.2 ns, which corresponds to the quantum
yield of 0.066 ± 0.013. (
Inset
) Global distribution (ten year average) of
chlorophyll concentrations in the boreal summer. The grey area
indicates oligotrophic regions with chlorophyll concentrations below 0.1
mg·m−3; this area covers ~30
%
of the global ocean.
First release: 7 January 2016 www.sciencemag.org (Page numbers not final at time of first release) 7
... The use of natural, or sun-induced chlorophyll a (Chl a) fluorescence (SICF) as an indicator of phytoplankton photophysiological status requires knowledge of the fluorescence quantum yield (Φ) and the factors that control its variability (Babin et al. 1996;Letelier et al. 1997;Maritorena et al. 2000;Abbott et al. 2001;Morrison 2003;Westberry and Siegel 2003;Schallenberg et al. 2008;Behrenfeld et al. 2009;Westberry et al. 2013;Browning et al. 2014;Lin et al. 2016). In situ Φ F is defined as the ratio of photons emitted as fluorescence to those absorbed by phytoplankton and is referred to as an apparent Φ F . ...
... Although ΦF can be influenced by macronutrient (nitrate, phosphate, silicate) limitation, for example, under phosphate limitation phytoplankton cells are unable to carry out photosystem repairs (Wykoff et al. 1998), Φ F is typically considered a poor proxy for macronutrient limitation when investigated with SICF (Schallenberg et al. 2008). On the other hand, limitation by the micronutrient iron, a vital element required for photosynthetic electron transport (Raven et al. 1999), is known to drive an increase in Φ F (Lin et al. 2016). This is due to a decrease in the number of functional reaction centers and an increase in the pool of light harvesting complexes (Strzepek et al. 2019), some of which may be energetically uncoupled (Greene et al. 1991;Schrader et al. 2011;Macey et al. 2014). ...
... The derivation of Φ F requires, besides accurate quantification of the fluorescence signal, knowledge of the spectral absorption capacity of phytoplankton and a fully characterized light field. Field studies of Φ F typically involve SICF measurements (Letelier et al. 1997;Maritorena et al. 2000;Morrison 2003;Schallenberg et al. 2008) or proxies derived from active fluorometry (Browning et al. 2014;Lin et al. 2016); however, the use of multiexcitation fluorometers in the derivation of Φ F has been proposed (Ostrowska 2012;Griffith et al. 2018). Multiexcitation fluorometers typically exploit fluorescence excitation spectra to define phytoplankton taxonomic groups based on signature accessory pigment composition (Sosik and Mitchell 1995;Johnsen et al. 1997), which is used to discriminate between phytoplankton species in mixed assemblages (Cowles et al. 1993;Beutler et al. 1998Beutler et al. , 2002Beutler et al. , 2003. ...
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... The excitation energy collected in the antenna complexes is transferred to the photosystems in a non-radiative way. At PSII, the energetic differences between excited core complex and peripheral FCPs are low which leads to an energetic continuum that allows energy transfer in all directions, even from PSII towards the peripheral antennas (Kuzminov & Gorbunov 2016;Schatz et al. 1987). After excitation of a PSII core Chl a dimer (P680), a pheophytin --P680 + intermediate is formed allowing a rereduction of P680 + by one single electron of the water-splitting complex via a tyrosine residue of D1 (Ferreira et al. 2004;Rappaport & Diner 2008;Telfer 2002). ...
... This decrease in σ(PSII) clearly indicates a reduction in the flux of energy to the PSII core, which provides photoprotection under supra-optimal light. While previously it has been shown that the decrease in σ(PSII) correlates to a certain degree with the NPQ capacity in different algal species (Giovagnetti & Ruban 2017;Koblížek et al. 2001;Kuzminov & Gorbunov 2016;Olaizola et al. 1994;Perkins et al. 2018;Tian et al. 2019;Xu et al. 2018), ...
... As Dt binds to LHC antenna proteins Wang et al. 2019) and Lhcx proteins are not part of the PSII core (Umena et al. 2011), the decrease in σ(PSII) is indicative of thermal dissipation of absorbed energy in the LHC antenna complexes, as originally proposed by Genty et al. (1990). Accordingly, analysis of picosecond lifetime kinetics revealed that the exposure to supra-optimal irradiances leads to functional modifications in both antennae and PSII reaction centers, but the thermal dissipation occurs only in the antennae (Kuzminov & Gorbunov 2016). Our results also showed that the slow phase of NPQ, which is activated under prolonged exposure to higher light levels, has no effect on σ(PSII). ...
... NPQ levels may vary significantly and therefore influence the heat dissipation rate in surface waters. However, when examining photosynthetic organisms in deeper layers under lower irradiance, heat dissipation is expected to be minimal and constant 30 . In this scenario, changes in the quantum yield of photochemistry (Φ p ) are inversely related to the quantum yield of fluorescence (Φ f ). ...
... This is a standard method for estimating light-harvesting efficiency in laboratory studies 31 . Using timecorrelated single-photon counting (TCSPC) technique to measure fluorescence lifetime in the picosecond time domain, we can quantitatively relate the fluorescence lifetime to the absolute quantum yield of fluorescence 13,14,30 ...
... Recent advances in TCSPC methods have allowed for fluorescence lifetime measurements of photosynthetic communities in situ 23,30,40 . These earlier studies tackled the lifetime of chlorophyll in surface water, an abundant and constitutive pigment in all photosynthetic systems. ...
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... The average algal cell in the global ocean funnels about 35% of absorbed light energy to the photosystem II (PSII) reaction centers where the water-splitting reaction occurs. The remaining ~65% of absorbed light energy is lost as heat or fluorescence (Kirk, 1994;Lin et al., 2016). The canonical step in photosynthesis uses light energy to extract electrons from water and simultaneously releases oxygen. ...
... This chapter focuses solely on single turnover variable fluorescence (ST-ChlF), the most common variant of variable fluorescence and the best suited for aquatic primary production. Other variable fluorescence variants not addressed here include pulse modulated fluorescence (PAM, Schreiber et al., 1986) and picosecond fluorescence decay kinetics (Lin et al., 2016). Section 9.2 provides a brief theoretical overview of ST-ChlF protocols and the derivation of primary ChlF parameters. ...
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The measurement of aquatic primary productivity (PP) is central to the quantitative understanding of the global biosphere, yielding critical insights into the role and magnitude of carbon, oxygen, and other bioactive element fluxes between the ocean, the geosphere, and the atmosphere. The accumulation of theoretical, methodological, and technological advances from this endeavor has led to the development of numerous approaches to measure oceanic PP, all with the common objective of quantifying the fluxes of reduced carbon into aquatic ecosystems. While these advances have furthered the understanding of carbon dynamics, from intracellular to global scales, it is notable that perhaps no single measurement in the suite of significant oceanographic observations exhibits as much methodological diversity and interpretive ambiguity
... The average algal cell in the global ocean funnels about 35% of absorbed light energy to the photosystem II (PSII) reaction centers where the water-splitting reaction occurs. The remaining ~65% of absorbed light energy is lost as heat or fluorescence (Kirk, 1994;Lin et al., 2016). The canonical step in photosynthesis uses light energy to extract electrons from water and simultaneously releases oxygen. ...
... This chapter focuses solely on single turnover variable fluorescence (ST-ChlF), the most common variant of variable fluorescence and the best suited for aquatic primary production. Other variable fluorescence variants not addressed here include pulse modulated fluorescence (PAM, Schreiber et al., 1986) and picosecond fluorescence decay kinetics (Lin et al., 2016). Section 9.2 provides a brief theoretical overview of ST-ChlF protocols and the derivation of primary ChlF parameters. ...
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... It was shown in [40] that the efficiency of phytoplankton photosynthesis is inversely proportional to the fluorescence value. It is mentioned in [41] that photochemical energy conversion is physiologically limited by nutrients, and the flh value reflects the photophysiological state of phytoplankton. Fluorescence is affected by nutrient deficiency [42]. ...
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