Abstract
Kleptoplasty or acquisition of chloroplasts from ingested photosynthetic organisms, is thought to be a key factor in determining the trophic requirements and carbon mineralization of foraminifera, consequently influencing their ecology, evolution, and calcification. However, the acquisition, maintenance, and functions of “stolen” chloroplasts (kleptoplasts) in foraminiferal cells have not been well characterized. Using molecular phylogeny and experimental measurements of oxygen flux and intracellular (vacuole) pH, we characterized aspects of kleptoplast origin and function in Planoglabratella opercularis (d’Orbigny), a rocky-shore benthic foraminifera. We determined that the kleptoplasts in P. opercularis are derived from various species of epiphytic diatoms. The acquisition of epiphytic diatoms is congruent with the behaviour of P. opercularis, which crawls on the thalli of coralline algae and grazes on the microalgae on the algal surface. Kleptoplasts were located near the host foraminiferal cell periphery, just under the pore plug, mainly along the dorsal side, which is important for oxygenic photosynthesis. The lifespan of kleptoplasts varied according to food availability and to the intensity and duration of light irradiation. Planoglabratella opercularis was able to capture not only diatom chloroplasts but also those from Chlorella. Kleptoplastids of diatom origin decreased in autofluorescence and were digested within 11 days under light in the absence of food. This suggests that host foraminifera frequently capture new diatoms to sustain kleptoplasts. Kleptoplastid autofluorescence was prolonged in the dark or 24:24-h light:dark cycle, and when food was available. Host foraminifera metabolized food to maintain the activity of kleptoplasts and effectively utilized photosynthetic products from both organic and inorganic materials in response to the ambient environment. This suggests that P. opercularis behaves as a mixotroph. Simultaneously, kleptoplasts maintain a high intracellular pH environment, indicating that foraminifera capture kleptoplasts not only to gain their photosynthates but also to control the intracellular pH levels to construct a high magnesian calcite test.
Highlights
Host–symbiont interactions, for example in endosymbiontbearing foraminifera, are thought to be a key factor for adaptation and a driving in evolution (Lee et al, 2010)
The aim of the study was to understand the acquisition and maintenance of kleptoplasts in the rocky-shore benthic foraminifera P. opercularis and to determine whether kleptoplasty is a key factor for foraminiferal ecology in the metabolic and adaptive mechanisms of this species
Configuration and Localization of Kleptoplasts To understand the acquisition and maintenance of kleptoplasts in the rocky-shore benthic foraminifera P. opercularis and to determine whether kleptoplasty is a key factor for foraminiferal ecology in the metabolic and adaptive mechanisms of this species, we observed that the cytoplasm of P. opercularis contained kleptoplasts (Figure 1A), but kleptoplastid division was not observed
Summary
Host–symbiont interactions, for example in endosymbiontbearing foraminifera, are thought to be a key factor for adaptation and a driving in evolution (Lee et al, 2010). Host foraminifera harbor different symbiotic microalgae as a result of different pathways utilized during foraminiferal evolution. The acquisition of endosymbionts and utilization of the organic materials they produce may enable foraminifera to adapt to an oligotrophic environment. In larger foraminifera, oxygen readily permeates the host cell due to photosynthesis by endosymbiotic algae. Compared with their smaller, nonendosymbiotic counterparts, larger foraminifera can produce more juveniles during asexual reproduction (Röttger, 1974), increasing their population size. Nonendosymbiotic counterparts, larger foraminifera can produce more juveniles during asexual reproduction (Röttger, 1974), increasing their population size In this manner, endosymbiosis promotes foraminiferal species diversity and facilitates foraminiferal adaptation to a range of environments
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