Abstract
Some shallow water benthic foraminifera are able to retain functional chloroplasts (kleptoplasts) from their food source, i.e. diatoms. Here we assessed the functionality of the kleptoplast xanthophyll cycle (XC, i.e. the main diatom short-term photo-regulation mechanism) and we surveyed Haynesina germanica kleptoplast pigment composition over time and at different light regimes. Six common diatom lipophilic pigments were detected, two chlorophylls (Chl a, Chl c) and four carotenoids (fucoxanthin and by-products, diadinoxanthin, diatoxanthin and β-carotene), the same pigment profile as the diatom species frequently isolated at the sampling site. The xanthophyll cycle (XC) was functional with kleptoplast diatoxanthin (DT) content increase with concomitant diadinoxanthin (DD) decrease after short term light exposure. DT/(DT+DD) and DT/DD ratios increased significantly in specimens exposed to low light and high light in comparison to specimens maintained in the dark. Specimens placed in very low light after the light treatments reverted to values close to the initial ones, suggesting that H. germanica XC is functional. A functional XC is an indication of H. germanica kleptoplasts capacity for short-term photo-protection from photo-oxidative damages caused by excess of light. Furthermore, the pigment survey suggests that H. germanica preserved some chloroplasts over a longer time than others and that pigment content is influenced by previous light history. Finally, the current study highlighted seasonal differences, with higher pigment contents in winter specimens (27.35 ± 1.30 ng cell-1) and lower in summer specimens (6.08 ± 1.21 ng cell-1), a quantitative and qualitative composition suggesting light acclimation to low or high light availability, according to the season.
Highlights
Benthic foraminiferal species have various particular physiological adaptations such as the capacity to store nitrate and to denitrify [1, 2] or to host endo- and ectosymbionts [3,4,5,6]
H. germanica pigment profiles were similar throughout experiment 1; total pigment content was lower in condition HL/very low light (VLL) compared to the other ones (Table 1)
If H. germanica is not sensitive to light [39] we can hypothesise that the xanthophyll cycle might be an important short-term photoprotective mechanism for the diatom kleptoplasts incorporated in the foraminifera cytosol. This was supported by our experiments, i.e. there was an increase in DT/DD ratios when foraminifera were exposed to light that was reversed when the same foraminifera were exposed to VLL (Fig 4), showing that the XC was functional at least in short-term time scales (i.e. 30 min). This is the first evidence of a functional xanthophyll cycle in kleptoplastic foraminifera and it is indicative of the presence of a short-term photoprotective mechanism protecting H. germanica kleptoplasts from photo-oxidative damages caused by excessive light
Summary
Benthic foraminiferal species have various particular physiological adaptations such as the capacity to store nitrate and to denitrify [1, 2] or to host endo- and ectosymbionts [3,4,5,6]. Among these adaptions developed by benthic foraminifera, some species have the ability to steal and sequester chloroplasts from diatoms and to keep them functional from days to many months [7,8,9,10,11,12,13,14,15,16,17,18] This process, called kleptoplasty [19], has been observed in intertidal as well as PLOS ONE | DOI:10.1371/journal.pone.0172678. This process, called kleptoplasty [19], has been observed in intertidal as well as PLOS ONE | DOI:10.1371/journal.pone.0172678 February 23, 2017
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