The biogenesis of Symbiodinium symbiosome in the host cells of the sea anemone, Aiptasia pulchella, involves retention of ApRab5 on and exclusion of ApRab11 from the organelle. One predicted consequence of this differential Rab association is the constant membrane fusion of symbiosomes with endocytic vesicles in the absence of parallel membrane retrieval and the subsequent formation of spacious symbiosomes, which nevertheless, contradicts the common perception. To solve this discrepancy, we determined whether membrane fusion occurs between symbiosomes and endocytic vesicles, and whether ApRab11-independent recycling is involved in symbiosome biogenesis. By using the biotin-avidin detection system, we found evidence for symbiosome-endocytic vesicle fusion. Cloning and characterization of ApRab4, an A. pulchella homolog of Rab4, showed that ApRab4 is associated with both the early endocytic and the perinuclear recycling compartments, and its normal function is required for the organization of the recycling compartments. Immunostaining localized ApRab4 to the symbiosome membrane, partially overlapping with ApRab5-decorated microdomains. Significantly, a treatment that impaired Symbiodinium photosynthesis also abolished symbiosome association of ApRab4. Furthermore, ApRab4 was quickly recruited to newly formed phagosomes, but prolonged association only occurred in those harboring live zooxanthelllae. We propose that ApRab4 retention on the symbiosome is an essential part of the mechanism for the biogenesis of Symbiodinium symbiosome.
Endosymbiosis between dinoflagellates and cnidarian hosts first occurred more than 200 million years ago; however, symbiosis-specific genes and cellular processes involved in the establishment, maintenance, and breakdown of endosymbiosis remain unclear. Therefore, this study aimed to identify the zooxanthellal genes associated with the aforementioned biological processes during endosymbiosis in Aiptasia-Symbiodinium endosymbionts. Here, zooxanthellae isolates were treated with 0.02% SDS to decrease potential host RNA contamination and to enhance the identification of novel symbiosis/nonsymbiosis-associated differentially expressed zooxanthellal genes through suppressive subtractive hybridization (SSH) and next-generation sequencing (NGS) methods. Consequently, among 214 symbiosis-specific transcripts identified herein that displayed identity to only 5.6% of host-derived transcripts, 64% were well-known functional genes. In the nonsymbiotic stage, 181 differentially expressed transcripts were identified, of which 64.1% belonged to well-known functional genes. BLAST revealed that 8 categories of cellular processes were significantly induced in symbiotic or nonsymbiotic zooxanthellae. Together with the results of quantitative analysis, the results revealed that photosynthesis, flagellate biosynthesis and motility, stress-induced responses, cell wall biosynthesis, starch synthesis and transport, lipid biosynthesis and metabolism, host/symbiont immune response, intercellular communication, cell growth, and cell cycle regulation were the major cellular processes occurring in symbiotic/nonsymbiotic stages. The present results provide insights into the mechanisms involved in regulating the different physiological processes in symbiotic/nonsymbiotic zooxanthellae and may guide future studies.
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