Innovative TEM-coupled approaches to study foraminiferal cells

Nomaki, Hidetaka; Lekieffre, Charlotte Madeleine Nicole; Escrig, Stéphane; Meibom, Anders; Yagyu, Shinsuke; Richardson, Elizabeth; Matsuzaki, Takashi; Geslin, Emmanuelle; Bernhard, Joan M.

doi:10.1016/j.marmicro.2017.10.002

Cited by 12 publications

(11 citation statements)

References 70 publications

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“…infiltration of 12 C-resin and fixatives within the samples and loss of soluble 13 C-enriched compounds (Musat et al 2014;Nomaki et al 2018). Thus, the 13 C-enrichment values of the different cellular compartments (including the starch grains) noted in this study are not the original enrichments values.…”

Section: Tem-nanosims Sample Preparationmentioning

confidence: 70%

“…In cnidarian symbiosis, translocation of photosynthates have been observed in the form of glycerol, glucose (or other hexoses), amino acids, or lipids (Muscatine et al 1967;Trench 1971Trench , 1979Hofmann and Kremer 1981;Kellogg and Patton 1983;Patton and Burris 1983;Whitehead 2003). Because the sample preparation we use for TEM-NanoSIMS analysis does not preserve soluble compounds (Nomaki et al 2018;Nuñez et al 2018), our study does not reveal information on the transfer of soluble photosynthates, such as glycerol, hexoses, and amino acids in the O. universa symbiotic system. However, lipids are largely preserved during sample preparation and can be studied.…”

Section: Photosynthate Translocation Inside the Host Cellmentioning

confidence: 88%

“…NanoSIMS image processing was carried out as described in LeKieffre et al (2017) and Nomaki et al (2018). Briefly, TEM images were aligned with corresponding NanoSIMS 12 C 14 N − images (Online Resource 1) using the software Look@NanoSIMS (Polerecky et al 2012), which allows a user to hand-draw regions of interest (ROIs) corresponding to different organelles (e.g., dinoflagellate starch grains, foraminiferal lipid droplets, and fibrillar bodies).…”

Section: Tem-nanosims Sample Preparationmentioning

confidence: 99%

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Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

et al. 2018

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Some species of planktic foraminifera inhabiting oligotrophic surface water environments are in an obligate symbiotic relationship with dinoflagellate microalgae, which can assimilate carbon (C) through photosynthesis. However, the mechanism and dynamics of C photosynthate translocation to the foraminiferal host, and related benefits for the dinoflagellates in this symbiotic association, are poorly constrained. As a consequence, the role of planktic foraminifera as autotroph organisms in ocean surface ecosystems is not well understood. Here, we performed pulse-chase experiments with 13 C-enriched dissolved inorganic carbon, followed by TEM and quantitative NanoSIMS isotopic imaging to visualize photosynthetic C assimilation by individual symbiotic dinoflagellates and subsequent translocation to their Orbulina universa host. Although most of the dinoflagellate population migrates out of the host endoplasm onto external spines during the day, our observations show that a small fraction remains inside the host cell during daytime. All symbionts, whether outside or inside the foraminifera cell, effectively assimilate C into starch nodules during daytime photosynthesis. At the onset of night, all dinoflagellates from the exterior spine-ectoplasm region migrate back into the foraminiferal cell. During the night, respiration by dinoflagellates and carbon translocation to the host, likely in the form of lipids, greatly reduces the abundance of starch in dinoflagellates. Dinoflagellate mitosis is only observed at night, with a substantial contribution of carbon fixed during the previous day contributing to the production of new biomass.

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Section: Tem-nanosims Sample Preparationmentioning

confidence: 70%

Section: Photosynthate Translocation Inside the Host Cellmentioning

confidence: 88%

Section: Tem-nanosims Sample Preparationmentioning

confidence: 99%

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Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

et al. 2018

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“…It is also noteworthy that Fv/Fm = 0 in N. labradorica , so photosystem II of the kleptoplasts was also not functional (measured by pulse amplitude modulated (PAM) fluorometry as in Jauffrais and colleagues (); data not shown). Note that chemical fixation protocols cause loss of soluble compounds and include infiltration of the fixed tissue with resin of normal C isotopic composition, which dilutes potential 13 C enrichment in the sample (Musat et al ., ; Kopp et al ., ; Nomaki et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution

Jauffrais

Lekieffre

Schweizer

et al. 2018

Environmental Microbiology

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Summary The assimilation of inorganic compounds in foraminiferal metabolism compared to predation or organic matter assimilation is unknown. Here, we investigate possible inorganic‐compound assimilation in Nonionellina labradorica, a common kleptoplastidic benthic foraminifer from Arctic and North Atlantic sublittoral regions. The objectives were to identify the source of the foraminiferal kleptoplasts, assess their photosynthetic functionality in light and darkness and investigate inorganic nitrogen and sulfate assimilation. We used DNA barcoding of a ~ 830 bp fragment from the SSU rDNA to identify the kleptoplasts and correlated transmission electron microscopy and nanometre‐scale secondary ion mass spectrometry (TEM‐NanoSIMS) isotopic imaging to study 13C‐bicarbonate, 15N‐ammonium and 34S‐sulfate uptake. In addition, respiration rate measurements were determined to assess the response of N. labradorica to light. The DNA sequences established that over 80% of the kleptoplasts belonged to Thalassiosira (with 96%–99% identity), a cosmopolitan planktonic diatom. TEM‐NanoSIMS imaging revealed degraded cytoplasm and an absence of 13C assimilation in foraminifera exposed to light. Oxygen measurements showed higher respiration rates under light than dark conditions, and no O2 production was detected. These results indicate that the photosynthetic pathways in N. labradorica are not functional. Furthermore, N. labradorica assimilated both 15N‐ammonium and 34S‐sulfate into its cytoplasm, which suggests that foraminifera might have several ammonium or sulfate assimilation pathways, involving either the kleptoplasts or bona fide foraminiferal pathway(s) not yet identified.

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“…Most cytological studies on foraminifera have been performed via microscopy techniques by observing the ultrastructure of the foraminiferal cell (e.g., Anderson & Lee, ; Jahn & Rinaldi, ; Ohno et al, ; Travis & Allen, ; Travis & Bowser, ; Tyszka et al, ) and have aimed to link the foraminiferal ultrastructure to physiological processes and environmental conditions (e.g., Bernhard et al, ; Bernhard & Bowser, ; Bernhard & Bowser, ; Frontalini et al, ; Goldstein & Richardson, ; Jauffrais et al, ; Koho et al, ). To study the adaptations of foraminiferal ultrastructure to habitat, researchers have developed different transmission electron microscopy‐coupled (TEM‐coupled) techniques (reviewed in Nomaki et al, ). Even though TEM‐based techniques allow scientists to obtain high‐resolution images, such methods commonly involve a lengthy series of preparation steps that can hamper their application for other purposes and excludes in vivo assessments.…”

Section: Introductionmentioning

confidence: 99%

Foraminiferal Ultrastructure: A perspective From Fluorescent and Fluorogenic Probes

et al. 2019

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Microscopy techniques have been widely applied to observe cellular ultrastructure. Most of these techniques, such as transmission electron microscopy, produce high‐resolution images, but they may require extensive preparation, hampering their application for in vivo examination. Other approaches, such as fluorescent and fluorogenic probes, can be applied not only to fixed specimens but also to living cells when the probes are nontoxic. Fluorescence‐based methods, which are generally relatively easy to use, allow visual and (semi)quantitative studies of the ultrastructural organization and processes of the cell under natural as well as manipulated conditions. To date, there are relatively few published studies on the nearly ubiquitous marine protistan group Foraminifera that have used fluorescent and fluorogenic probes, despite their huge potential. The aim of the present contribution is to document the feasible application of a wide array of these probes to foraminiferal biology. More specifically, we applied fluorescence‐based probes to study esterase activity, cell viability, calcium signaling, pH variation, reactive oxygen species, neutral and polar lipids, lipid droplets, cytoskeleton structures, Golgi complex, acidic vesicles, nuclei, and mitochondria in selected foraminiferal species.

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Innovative TEM-coupled approaches to study foraminiferal cells

Cited by 12 publications

References 70 publications

Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution

Foraminiferal Ultrastructure: A perspective From Fluorescent and Fluorogenic Probes

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