Assessment of algal photosynthesis in planktic foraminifers by fast repetition rate fluorometry

Fujiki, Tetsuichi; Takagi, Hirofumi; Kimoto, Katsunori; Kurasawa, Atsushi; Yuasa, Takahito; Mino, Yoshihisa

doi:10.1093/plankt/fbu083

Cited by 19 publications

(58 citation statements)

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“…When functional chlorophyll was detected in a specimen, then the maximum fluorescence (Fm) value was used to estimate chlorophyll a (Chl a) content of the specimen based on a linear relationship between Fm and Chl a (cf. Fujiki et al, 2014;Takagi et al, 2016). Calibration line was established for each FRR fluorometer.…”

Section: And 4)mentioning

confidence: 99%

“…These methods have been used in benthic symbiont-bearing foraminifera (e.g., Uthicke, 2006;Schmidt et al, 2011;Ziegler and Uthicke, 2011) and recently successfully adapted for application on single specimens of living planktonic foraminifera (Fujiki et al, 2014;Takagi et al, 2016Takagi et al, , 2018. An active chlorophyll fluorometry performs non-destructive and non-invasive measurements of algal physiology based on real-time variable fluorescence profiles (Kolber and Falkowski, 1993), allowing us to quantify chlorophyll a content of a specimen, the health of its symbionts and their light-level adaptation (Fujiki et al, 2014;Takagi et al, 2018). The measurements can be performed almost immediately after collection, with minimal manipulations, thus minimizing damage to the foraminifera and circumventing culturing stress-induced artifacts.…”

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Characterizing photosymbiosis in modern planktonic foraminifera

Takagi¹,

Kimoto²,

Fujiki³

et al. 2019

Preprint

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Abstract. Photosymbiosis has played a key role in the diversification of foraminifera and their carbonate production through geologic history. However, identification of photosymbiosis in extinct taxa remains challenging and even among the extant species the occurrence and functional relevance of photosymbiosis remains poorly constrained. Here, we investigate photosymbiosis in living planktonic foraminifera by measuring active chlorophyll fluorescence with fast repetition rate fluorometry. This method provides unequivocal evidence for the presence of photosynthetic capacity in individual foraminifera and it allows us to characterize multiple features of symbiont photosynthesis including chlorophyll a (Chl a) content, potential photosynthetic activity (Fv&#8201;/&#8201;Fm), and light absorption efficiency (&#963;PSII). To obtain robust evidence for the occurrence and importance of photosymbiosis in modern planktonic foraminifera, we conducted measurements on 1266 individuals from 30 species of the families Globigerinidae, Hastigerinidae, Globorotaliidae, and Candeinidae. Among the studied species, 19 were recognized as symbiotic and 11 as non-symbiotic. Of these, six species were newly confirmed as symbiotic and five as non-symbiotic. Photosymbiotic species have been identified in all families except the Hastigerinidae. A significant positive correlation between test size and Chl a content, found in 16 species, is interpreted as symbiont growth scaled to the growth of the host, consistent with persistent possession of symbionts through the lifetime of the foraminifera. The remaining three symbiont-bearing species did not show such a relationship, and their Fv&#8201;/&#8201;Fm values were comparatively low, indicating that their symbionts do not grow once acquired from the environment. The objectively quantified photosymbiotic characteristics have been used to design a metric of photosymbiosis, which allows the studied species to be classified along a gradient of photosynthetic activity, providing a framework for future ecological and physiological investigations of planktonic foraminifera.

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confidence: 99%

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confidence: 99%

Characterizing photosymbiosis in modern planktonic foraminifera

Takagi¹,

Kimoto²,

Fujiki³

et al. 2019

Preprint

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“…Firstly, the empirical proxy relationships we apply to our data have been calibrated using bulk shell compositions and over a range of seawater compositions that are much narrower than our DIC experiments. Secondly, the rates of photosynthesis and respiration are constant in the model, although they have been observed to change daily with changes in symbiont productivity (Spero and Parker, 1985) and throughout the foraminifer's ontogeny as it grows and symbiont numbers increase (Fujiki et al 2014;Spero and Parker, 1985;Takagi et al, 2016). This might explain why B/Ca and U/Ca banding overlies broader compositional trends that occur with shell thickening over multiple days of growth (Fig.…”

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confidence: 99%

Calcification rate and shell chemistry response of the planktic foraminifer Orbulina universa to changes in microenvironment seawater carbonate chemistry

Holland

Eggins

Hönisch

et al. 2017

Earth and Planetary Science Letters

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We use LA-ICP-MS depth profiling to explore the sensitivity of shell chemistry of the symbiotic planktic foraminifer Orbulina universa to diurnal changes in the holobiont physiology, over a wide range of seawater pH and DIC compositions. B/Ca and U/Ca vary in concert with diurnal Mg/Ca banding, forming compositional bands that are qualitatively consistent with physiological modification of seawater carbonate chemistry (pH, [B(OH) 4-/HCO 3-] and [CO 3 2-]) within the foraminiferal microenvironment by the net effects of photosynthesis, respiration and calcification. The amplitude of B/Ca banding broadly conforms to banding predicted using the bulk-shell B/Ca sensitivity to the carbonate chemistry changes in the foraminiferal microenvironment. U/Ca banding tends to be greater than predicted using the published bulk-shell sensitivity of this proxy to carbonate chemistry. This either suggests that carbonate chemistry changes in the foraminiferal microenvironment are greater than predicted by modelling and/or the published bulk shell calibration does not accurately reflect the U/Ca sensitivity at the micro-scale. A fourfold increase in seawater DIC composition (1026 to 4019 µmol kg-1) is associated with significant increases in Sr/Ca and Mg/Ca partitioning, and a decrease in Mn/Ca partitioning into shell calcite. The accompanying fourfold increase in calcite saturation produces only a twofold increase in

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“…Symbionts of type II were ultrastructurally distinct from type I, but it was not possible to distinguish them as haptophytes or chrysophytes (Faber et al 1988 ). Recently, a study obtained the 18S rDNA sequence of the symbiont from hosts collected in the North Pacifi c and showed that the symbiont of type II is related to the genus Pelagomonas (Fujiki et al 2014 ).…”

Section: Planktonic Foraminiferamentioning

confidence: 99%

Photosymbiosis in Marine Planktonic Protists

2015

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Some of the most enigmatic components in the plankton are the diverse eukaryotic protists that live in close association with one or more partners. Mutualistic and commensal planktonic interactions are most commonly encountered in the oligotrophic open ocean at tropical and subtropical latitudes. They are functionally and ecologically distinct, and involve a great taxonomic diversity of single-celled partners. Protists like Foraminifera, Radiolaria, dinofl agellates and diatoms can all harbor microalgal symbionts of eukaryotic and prokaryotic origin inside (endosymbiosis) and/or outside (ectosymbiosis) their cytoplasm. Such symbioses (photosymbioses) combine phototrophy, heterotrophy and sometimes dinitrogen (N 2 ) fi xation (reduction of N 2 to ammonium). Symbiotic microorganisms therefore represent an important component of marine ecosystems and play a role in the food web and biogeochemical cycling (e.g., carbon and nitrogen). Despite their important ecological function and early recognition in the late nineteenth century, our knowledge about the diversity, distribution, and metabolic exchanges for many of the photosymbioses remains rudimentary compared with the other marine and terrestrial symbioses. Recent technical advances in single-cell genomics and imaging have greatly improved our understanding about planktonic symbioses. This review aims to present and compare many eukaryote-eukaryote and eukaryote-prokaryote photosymbioses described so far in the open ocean with an emphasis on their ecology and potential function in the ecosystem.

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Assessment of algal photosynthesis in planktic foraminifers by fast repetition rate fluorometry

Cited by 19 publications

References 17 publications

Characterizing photosymbiosis in modern planktonic foraminifera

Characterizing photosymbiosis in modern planktonic foraminifera

Calcification rate and shell chemistry response of the planktic foraminifer Orbulina universa to changes in microenvironment seawater carbonate chemistry

Photosymbiosis in Marine Planktonic Protists

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