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T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
Figure 1. Spectral reflectance signatures of Haynesina germanica,
Ammonia tepida and of a benthic diatom in relative units (x axis
legend: Wavelength (nm)).
Figure 2. Illustration of Haynesina germanica chloroplast content
at the beginning (a) and at the end of the experiment for the three ex-
perimental conditions, Dark (b), Low Light (c) and High Light (d).
Size and biovolume
Higher colour scale values correspond to foraminifera emittingmore fluorescence and likely containing more chlorophyll a; flu- Ammonia tepida specimens were larger than H. german- orescence in pixel values between 0 and 255, (scale bar = 50 µm).
ica with a mean maximal elongation of 390 ± 42 µm(SD, n = 34) and 366 ± 45 µm (SD, n = 122), respectively(p < 0.01, F121,33 = 1.15). This resulted in cytoplasmic bio- lis) showing that the differences in chlorophyll a fluores- volumes equal to 1.20 × 107 ± 3.9 × 106 µm3 (SD) and cence were significant (p < 0.01, Df = 3, Fig. 3). It is also 1.01 × 107 ± 3.65 × 106 µm3 (SD), respectively.
noteworthy to mention that there was a large individual vari-ability within each treatment leading to large standard errors in spite of the number of replicates (n = 30).
Fresh Haynesina germanica and A. tepida showed very dif- ferent spectral reflectance signatures (Fig. 1). Haynesina ger- between the two species. Ammonia tepida did not manica showed a typical diatom spectral signature with high show any net oxygen production although respiration reflectance in the infrared region (> 740 nm) and clear ab- rates measured at 300 µmol photons m−2 s−1 were lower sorption features around 585, 630 and 675 nm; the absorption (2485 ± 245 pmol O2 cell−1 d−1) than the ones measured feature around 675 nm corresponds to the presence of chloro- in the dark (3531 ± 128 pmol O2 cell−1 d−1) (F2,2 = 3.7, phyll a; the 585 nm feature is the result of fucoxanthin and p = 0.02). Haynesina germanica showed lower dark res- the 630 nm absorption feature is the result of chlorophyll c piration rates (1654 ± 785 pmol O2 cell−1 d−1) and oxygen (arrows, Fig. 1). Ammonia tepida showed no obvious pig- production quickly increased with irradiance, showing ment absorption features apart from 430 nm (Fig. 1).
no evidence of photoinhibition within the light range Epifluorescence images showed a clear effect of the dif- used (Fig. 4). Compensation irradiance (Ic) was reached ferent light treatments (Dark, Low Light, Hight Light) on H. very quickly, as low as 24 µmol photons m−2 s−1 (95 % germanica chlorophyll fluorescence (Fig. 2). Visual observa- coefficient bound: 17–30 µmol photons m−2 s−1, values cal- tions showed a clear decrease in chlorophyll fluorescence for culated from the fitted model Eq. 4) and the half-saturation the LL and HL treatments from the beginning of the experi- constant (Ek) was also reached at very low light levels, ment (Fig. 2a) to the end of a 7-day period of light exposure i.e. at 17 µmol photons m−2 s−1. No photoinhibition was (Fig. 2c and d, respectively). Samples kept in the dark did not observed under the experimental light conditions (0 to show an obvious decrease but showed a more patchy distribu- 300 µmol photons m−2 s−1), which resulted in an estimation tion compared to the beginning of the experiment (Fig. 2b).
of ∼ 2800 pmol O2 cell−1 d−1 for maximum photosyn- This was confirmed by a non-parametric test (Kruskal Wal- thetic capacity. The P -I curve initial slope at limiting Biogeosciences, 13, 2016
T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
Table 1. Light and dark respiration rates (pmol O2 cell−1 d−1)
± SD of Haynesina germanica in the three experimental conditions
(Dark, Low Light and High Light) at the end of the experiment (Df,
degree of freedom, PFD photon flux density).
Respiration rate (pmol O2 cell−1 d−1) Figure 3. Mean chlorophyll a fluorescence (±SE, n = 30) at the end
ent between conditions (p < 0.001), with significantly lower for the three experimental conditions (Dark, Low Light and High respiration rates of specimens incubated under High Light Light) and the beginning (T0) of the experiment using Haynesina conditions than those under Dark and Low Light conditions germanica. Higher mean values likely corresponded to foraminiferacontaining more chlorophyll.
(p < 0.05, Fisher's LSD test).
PAM fluorescence rapid light curve (RLC) parameters (α, rETRmax, Ek and Eopt) showed significant differences be-tween foraminiferal species and over the duration of the ex-periment (Figs. 5 and 6). Highest rETRmax, α and Eopt werealways observed in H. germanica. After only one starvationday A. tepida RLC parameters dropped to zero or close tozero. In contrast, H. germanica RLC parameters showed aslow decrease throughout the experiment (Figs. 5 and 6) withrETRmax and α decreasing from 6 to 4 and 0.22 to 0.15,respectively (Figs. 6a and b). The parameters Ek and Eoptstayed constant over the 7 days of the experiment, with val-ues oscillating around 30 and 90, respectively (Fig. 6c andd).
PSII maximum quantum yields (Fv/Fm) were clearly af- fected by light and time (Fig. 7). Both species showed highinitial Fv/Fm values, i.e. > 0.6 and 0.4 for H. germanica andA. tepida, respectively (Fig. 7). However, while A. tepida Fv/Fm values quickly decreased to zero after only one starva- (pmol O2 cell−1 d−1) as a function of the photon flux density (PFD, tion day, H. germanica exhibited a large variability between µmol photons m−2 s−1). The half-saturation constant, Ek, was light conditions (D, LL, HL) throughout the duration of the found at 17 (13–21), the dark respiration, Rd, at 1654 (1522–1786) experiment (Fig. 7); decreasing from 0.65 to 0.55 in darkness pmol O2 cell−1 d−1 and the maximum photosynthetic capacity, (D), from 0.65 to 0.35 under low light (LL) conditions and Pm, at 2845 (2672–3019) pmol O2 cell−1 d−1. The Ic, calculated from 0.65 to 0.20 under high light (HL). Using these Fv/Fm compensation irradiance (24 (17–30) µmol photons m−2 s−1). Theadjusted R2 of the model was equal to 0.998, n = 3.
decreases, H. germanica kleptoplast functional times wereestimated between 11 and 21 days in the dark (D), 9–12 daysin low light (LL) and 7–8 days in high light (HL), depending irradiance (α) was estimated at 70 pmol O on whether or not an exponential or linear model was applied.
(µmol photons m−2 s−1)−1 (95 % coefficient bound: 58–88).
Ammonia tepida chloroplast functional times were estimated Oxygen measurements carried out at the end of the exper- between 1 and 2 days (exponential and linear model, respec- iment (T7) showed significant different dark and light res- tively) and light exposure reduced the functional time to less piration rates, with light respiration being lower than dark than 1 day (data not shown).
respiration but not reaching net oxygen production rates (D,LL, HL) (Table 1). Moreover, respiration rates were differ- Biogeosciences, 13, 2016
T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
ida was found to carry out aerobic respiration, but respirationrates measured at 300 µmol photons m−2 s−1 were lower thanthose measured in the dark. We thus suppose that in A. tepidaoxygen production by ingested diatom or chloroplasts mightbe possible, provided that this species is constantly suppliedwith fresh diatoms. However, another possibility to explainthis reduction in oxygen consumption could be a decrease ofits metabolism or activity under light exposure. The light anddark oxygen production or consumption values measured forboth species are in accordance with previous studies (Geslinet al., 2011).
According to Lopez (1979), measured oxygen data can be used to estimate H. germanica carbon fixation rates. Thus,using 1000 pmol O2 cell−1 d−1 at 300 µmol photons m−2 s−1,∼ 200 to 4000 cells per 50 cm3 in the top 0.5 cm (Morvanet al., 2006; Bouchet et al., 2007) and assuming that photo-synthesis produced one mol O2 per mol of C fixed, H. ger- Figure 5. Rapid light curves (RLC, n = 3) expressed as the relative
manica primary production would be between 1.8 × 10−5 electron transport rate (rETR) as a function of the photosynthetic and 4.0 × 10−4 mol C m−2 d−1. This is a very low value active radiation (PAR in µmol photons m−2 s−1) of Haynesina ger- compared to microphytobenthos primary production in At- manica (black lines) and Ammonia tepida (black dashed lines) dur- lantic mudflat ecosystems, which usually range from 1.5 to ing the 7 days of the experiment.
5.9 mol C m−2 d−1 (e.g. Brotas and Catarino, 1995, reviewedin MacIntyre et al., 1996). The estimated values representthus less than 0.1 % of microphytobenthos fixated carbon and are in the same range of values than what has been describedby Lopez (1979) using 14C radioactive tracers. These results should be interpreted with caution because a wide variety offactors probably affect H. germanica in situ primary produc- Our results clearly show that only H. germanica was capable tion, e.g. diatom availability, kleptoplast densities, nutrient of carrying out net photosynthesis. Haynesina germanica had supply, light exposure, sea water turbidity, local biogeochem- typical diatom reflectance spectra (Fig. 1), showing the three ical processes and migration capability are all factors that major diatom pigment absorption features: chlorophyll a, can potentially affect H. germanica kleptoplast functionality.
chlorophyll c, and fucoxanthin (Meleder et al., 2003, 2013; Nevertheless, although carbon fixation seems not to be rele- Jesus et al., 2008; Kazemipour et al., 2012). Conversely, in vant at a global scale, the oxygen production could be impor- A. tepida these absorption features were not detected, sug- tant at a microscale and relevant in local mineralization pro- gesting that diatom pigments ingested by this species were cesses in/on mudflat sediments (e.g. iron, ammonium, man- quickly digested and degraded to a degree where they were no longer detected by spectral reflectance measurements.
At sampling time (T0) H. germanica rETR and Fv/Fm These non-destructive reflectance measurements are thus in values were similar to microphytobenthic species (i.e.
accordance with other studies on benthic foraminifera pig- Fv/Fm > 0.65) (Perkins et al., 2001), suggesting that the klep- ments by HPLC showing that H. germanica feed on benthic toplast PSII and electron transport chain were not much af- diatoms (Knight and Mantoura, 1985). Similarly, Knight and fected after incorporation in the foraminifers' cytoplasm. In Mantoura (1985) also detected higher concentrations and less contrast, A. tepida Fv/Fm and RLC parameters were already degraded diatom pigments in H. germanica than in A. tepida. much lower on the sampling day and quickly decreased to Furthermore, H. germanica has the ability to pro- almost zero within 24 h, suggesting that plastids were not duce oxygen from low to relatively high irradiance, stable inside the A. tepida cytoplasm. Complete diatoms in- as shown by the low compensation point (Ic) of side A. tepida were already observed in feeding studies (Le 24 µmol photons m−2 s−1 and the high onset of light sat- Kieffre, pers. com), this low Fv/Fm value might thus come uration (> 300 µmol photons m−2 s−1) (Fig. 4). Thus, H. from recently ingested diatoms by A. tepida. Fv/Fm has pre- germanica seems to be well adapted to cope with viously been used to determine kleptoplast functional times the high light variability observed in intertidal sedi- and to follow decrease in kleptoplast efficiency in other klep- ments that can range from very high irradiance levels toplastic organisms, e.g. the sea slug Elysia viridis (Vieira (> 1000 µmol photons m−2 s−1) at the surface of the sediment et al., 2009). Fv/Fm measurements carried out on H. ger- during low tide to very low levels within the sediment matrix manica at different light conditions showed that light had a or during high tide in turbid mudflat waters. Ammonia tep- significant effect on the estimation of kleptoplast functional Biogeosciences, 13, 2016
T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
Figure 6. Rapid light curve (RLC, n = 3) parameters for Haynesina germanica (Dark-RLC) and Ammonia tepida maintained in the dark
during the experiment, Alpha is the initial slope of the RLC at limiting irradiance, rETRmax is the maximum relative electron transport rate,
Ek is the light saturation coefficient and Eopt is the optimum light, all of them were estimated by adjusting the experimental data to fit the
model of Platt et al. (1980).
time, with the longest functional time estimated at 21 days for was amplified in low and high irradiance and it should dark conditions. This time frame would qualify H. german- be pointed out that the actual light level of the HL treat- ica as a long-term kleptoplast retention species (Clark et al., ment (i.e. 70 µmol photons m−2 s−1) is very low compared 1990); however, our 7 days estimation for the high light treat- to irradiances in their natural environment, which are easily ment would place H. germanica in the medium-term reten- going above 1000 µmol photons m−2 s−1, showing that the tion group. This clearly shows that light exposure has an im- foraminifera kleptoplasts lack the high photoregulation ca- portant effect on this species kleptoplast functionality. Con- pacity exhibited by the benthic diatoms that they feed upon cerning A. tepida, the short dark diatom or chloroplast func- (Cartaxana et al., 2013). This is consistent with the observa- tional time (< 2 days) places this species directly in the short tion at the end of the experiment that no net oxygen produc- or medium-term retention group.
tion was occurring under the different light conditions. Nev- Additionally, H. germanica kept in darkness showed a ertheless, a small difference was still found between dark and slow decrease of the RLC parameters, α and rETRmax, light respiration (Table 1), suggesting that some oxygen pro- throughout the 7 experimental days; this decrease is likely duction was still occurring but it was not sufficient to com- related to overall degradation of the light-harvesting com- pensate for the respiration oxygen consumption. We also no- plexes and of other components of the photosynthetic ap- ticed that the respiration was higher in the foraminifera main- paratus, which gradually induced a reduction of light har- tained in low light and dark conditions in comparison to the vesting efficiency and of carbon metabolism. This decrease high light foraminifera. In the line of the lower Fv/Fm values Biogeosciences, 13, 2016
T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
This fundamental difference could explain why kleptoplastfunctional times are much longer in N. stella, reaching up to1 year in specimens kept in darkness (Grzymski et al., 2002).
On the other hand, it has been shown that isolated chloro-plasts are able to function for several months in Sacoglossansea slugs provided with air and light in aquaria (Green etal., 2001; Rumpho et al., 2001), which demonstrates the ex-istence of interactions between the kleptoplast and the hostgenomes, and/or of mechanisms facilitating and supportingsuch long-lasting associations. In H. germanica exposed tohigh light it is also possible that reactive oxygen species(ROS) production rates of the sequestered chloroplasts mightexceed the foraminifera capacity to eliminate those ROS,thus inducing permanent damage to the foraminifera. ThisROS production could also eventually damage the klepto-plasts resulting in higher kleptoplast degradation rates.
Figure 7. Maximum quantum efficiency of the photosystem II
Possible advantages of kleptoplasty for intertidal
(Fv/Fm, n = 3) during the experiment for the different applied con- ditions (Dark, Low Light and High Light) and species (Haynesinagermanica and Ammonia tepida).
Much is still unknown about the relationship between klep-toplastic benthic foraminifera and their sequestered chloro- observed, this suggests that kleptoplasts and possibly other plasts. The relevance of the photosynthetic metabolism com- metabolic pathways might have been damaged by the excess pared to predation or organic matter assimilation is unknown; light. Clearly, in H. germanica light exposure had a strong however, it would be of great interest to understand the klep- effect on PSII maximum quantum efficiency and on the re- toplast role in the foraminiferal total energy budget. Oxy- tention of functional kleptoplasts (Fig. 7), which can explain genic photosynthesis comprises multiple reactions leading the absence of net oxygen production after the 7 days of the to the transformation of inorganic carbon to carbohydrates.
experiments. Comparable results for H. germanica were also However, to produce these carbohydrates all the light-driven obtained by counting the number of chloroplasts over time reactions have to be carried out, as well as the Calvin cy- with cells exposed or not to light (Lopez, 1979). One of the cle reactions. With fresh kleptoplasts this hypothesis seems most probable explanations for the observed Fv/Fm decrease possible (e.g. Lopez, 1979), especially if the plastid proteins is the gradual inactivation of the protein D1 in PSII reaction are still present and functional. However, we showed that the centres. This protein is an essential component in the electron maximum quantum efficiency of the PSII decreased quickly transport chain and its turnover rate is frequently the limiting under light exposure, suggesting that substantial direct carbo- factor in PSII repair rates (reviewed in Campbell and Tyys- hydrate production is unlikely without constant chloroplast tjärvi, 2012). Normally, protein D1 is encoded in the chloro- replacement. Conversely, the production of intermediate pho- plast and is rapidly degraded and resynthesized under light tosynthetate products such as adenosine triphosphate (ATP) exposure with a turnover correlated to irradiance (Tyystjärvi and nicotinamide adenine dinucleotide phosphate (NADPH) and Aro, 1996). However, although D1 is encoded by the could be possible and would be of metabolic value for the chloroplast genome, its synthesis and concomitant PSII re- foraminifera. It is also possible that in situ the foraminifera covery require further proteins that are encoded by the algal have better photoregulation capacities. Not only will they nuclear genome (Yamaguchi et al., 2005). Thus, when D1 have easy access to fresh diatom chloroplasts, as H. german- turnover is impaired it will induce an Fv/Fm decrease corre- ica is mainly living in the first few millimetres of the super- lated to irradiance (Tyystjärvi and Aro, 1996) consistent to ficial sediment (Alve and Murray, 2001; Thibault de Chan- what was observed in the present study. In another deep sea valon et al., 2015), but they will also have the possibility of benthic species (Nonionella stella) the D1 and other plastid migrating within the sediment (Gross, 2000) using this be- proteins (RuBisCO and FCP complex) were still present in havioural feature to enhance their photoregulation capacity, the foraminifer 1 year after sampling (Grzymski et al., 2002).
similar to what is observed in benthic diatoms from micro- This shows that some foraminifera can retain both nuclear phytobenthic biofilms (e.g. Jesus et al., 2006; Mouget et al., (FCP) and chloroplast (D1 and RuBisCO) encoded proteins.
2008; Perkins et al., 2010). However, below the photic limit However, contrary to H. germanica, N. stella lives in deeper (max 2 to 3 mm in estuarine sediments reviewed in MacIn- environments never exposed to light and thus is unlikely to tyre et al., 1996; Cartaxana et al., 2011) it is unlikely that carry out oxygenic photosynthesis (Grzymski et al., 2002).
oxygenic photosynthesis will occur, even if live H. german- Biogeosciences, 13, 2016
T. Jauffrais et al.: Effect of light on photosynthetic efficiency of sequestered chloroplasts
ica are also found below this limit (Thibault de Chanvalon et distribution of living benthic foraminifera: First insight from ax- al., 2015; Cesbron et al., 2016).
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