Fine structure of the foraminifer Haynesina germanica (Ehrenberg) and its sequestered chloroplasts

Abstract The common, shallow-water foraminiferan Haynesina germanica (Ehrenberg) is one of a growing number of benthic rotalids known to acquire phototrophy through chloroplast retention (kleptoplasty). This species is broadly distributed, tolerant to a range of environmental conditions, and has been identified as a potential bioindicator of moderately polluted settings. This study was undertaken to better understand the fine structural relationships of this foraminiferan and its sequestered chloroplasts. Individuals were selected from fresh field collections and prepared for transmission electron microscopy (TEM) using high pressure freezing followed by freeze substitution (HPF/FS). This method is well-known for its high-resolution of cellular structure without many of the potential artifacts introduced by standard TEM chemical fixation. Features of the sequestered chloroplasts are consistent with those of diatoms, and pennate diatoms are the most likely source. The sequestered chloroplasts observed in H. germanica are surrounded by five membranes: the four chloroplast membranes of the diatom and an encompassing, outer vacuolar membrane of the foraminifer. Most of the chloroplast-containing vacuoles include a single chloroplast, but some contain up to three. The chloroplasts examined have numerous lamellae, each consisting of three thylakoids. The pyrenoid is traversed by a single lamella that contains a single thylakoid. Storage granules are present in some chloroplasts. Food vacuoles, common in many smaller benthic foraminifera, are rare in this species, which is consistent with its utilization of acquired phototrophy as documented by others. Both uninucleate (typically a gamont) and multinucleate (typically an agamont) individuals were observed, suggesting that this species has an alternation of generations like most benthic foraminifera. Other features of the cell body (e.g., abundant mitochondria, active Golgi bodies, multivesicular bodies, peroxisomes) are consistent with its occurrences in shallow-water, aerobic settings. In addition, fibrillar vesicles are common as are small pyriform electron-dense bodies of unknown origin or function. Vesicles that appear to accumulate wastes are also common.