Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats

Abstract

Assimilation, sequestration and maintenance of foreign chloroplasts inside an organism is termed "chloroplast sequestration" or "kleptoplasty". This phenomenon is known in certain benthic foraminifera, in which such kleptoplasts can be found both intact and functional, but with different retention times depending on foraminiferal species. In the present study, seven species of benthic foraminifera (Haynesina germanica, Elphidium williamsoni, E. selseyense, E. oceanense, E. aff. E. crispum, Planoglabratella opercularis and Ammonia sp.) were collected from shallow-water benthic habitats and examined with transmission electron microscope (TEM) for cellular ultrastructure to ascertain attributes of kleptoplasts. Results indicate that all these foraminiferal taxa actively obtain kleptoplasts but organized them differently within their endoplasm. In some species, the kleptoplasts were evenly distributed throughout the endoplasm (e.g., H. germanica, E. oceanense, Ammonia sp.), whereas other species consistently had plastids distributed close to the external cell membrane (e.g., Elphidium williamsoni, E. selseyense, P. opercularis).Chloroplast degradation also seemed to differ between species, as many degraded plastids were found in Ammonia sp. and E. oceanense compared to other investigated species. Digestion ability, along with different feeding and sequestration strategies may explain the differences in retention time between taxa. Additionally, the organization of the sequestered plastids within the endoplasm may also suggest behavioral strategies to expose and/or protect the sequestered plastids to/from light and/or to favor gas and/or nutrient exchange with their surrounding habitats.

Compound‐specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky‐shore environments

“…crispum in accord with Jauffrais et al. () because our nucleotide sequence data are different from the European E . crispum phylotype S11 (Darling et al., ).…”

“…patelliformis , and A . quadrangularis , harbored kleptoplasts from diatoms (Supporting information Table ; Table ; Figure a–d) (Jauffrais et al., ). Planoglabratella opercularis acquired chloroplasts from epiphytic diatoms, such as G .…”

“…opercularis (Figure a), whereas kleptoplasts spread throughout the entire cell cytoplasm in E . crispum (Figure e) (Jauffrais et al., ). In such cases, the foraminifera digest the diatom‐derived cytoplasm and organelles, but they can retain kleptoplasts and chloroplast‐like structures of captured microalgae in their food vacuoles.…”

“…Detailed procedures of preparation of samples for TEM have been provided by Jauffrais et al. () and Tsuchiya et al. ().…”

Foraminiferal Ultrastructure: A perspective From Fluorescent and Fluorogenic Probes

“…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, ).…”