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Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs, Plakobranchus ocellatus.

ABSTRACT: Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug, Plakobranchus ocellatus, and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the phenotype acquisition without horizontal gene transfer.

SUBMITTER: Maeda T

PROVIDER: S-EPMC8079154 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes.

Project description:Sacoglossan sea slugs are unique in the animal kingdom in that they sequester and maintain active plastids that they acquire from the siphonaceous algae upon which they feed, making the animals photosynthetic. Although most sacoglossan species digest their freshly ingested plastids within hours, four species from the family Plakobranchidae retain their stolen plastids (kleptoplasts) in a photosynthetically active state on timescales of weeks to months. The molecular basis of plastid maintenance within the cytosol of digestive gland cells in these photosynthetic metazoans is yet unknown but is widely thought to involve gene transfer from the algal food source to the slugs based upon previous investigations of single genes. Indeed, normal plastid development requires hundreds of nuclear-encoded proteins, with protein turnover in photosystem II in particular known to be rapid under various conditions. Moreover, only algal plastids, not the algal nuclei, are sequestered by the animals during feeding. If algal nuclear genes are transferred to the animal either during feeding or in the germ line, and if they are expressed, then they should be readily detectable with deep-sequencing methods. We have sequenced expressed mRNAs from actively photosynthesizing, starved individuals of two photosynthetic sea slug species, Plakobranchus ocellatus Van Hasselt, 1824 and Elysia timida Risso, 1818. We find that nuclear-encoded, algal-derived genes specific to photosynthetic function are expressed neither in P. ocellatus nor in E. timida. Despite their dramatic plastid longevity, these photosynthetic sacoglossan slugs do not express genes acquired from algal nuclei in order to maintain plastid function.

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Project description:We present the complete mitochondrial genome sequence of Plakobranchus cf. ocellatus (Heterobranchia: Sacoglossa), a so-called 'solar-powered' sea slug with long-term retention of chloroplasts. The mitochondrial genome was 14,177?bp in length containing the standard set of 13 protein-coding genes, 2 rRNAs, and 22 tRNAs. The base composition of 27.3% A, 15.6% C, 18.6% G, and 38.5% T showed a strong A?+?T bias. The genome organization of P. cf. ocellatus is identical to the other sacoglossan mitogenomes sequenced so far, except for Ascobulla fragilis.

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Algivore or phototroph? Plakobranchus ocellatus (Gastropoda) continuously acquires kleptoplasts and nutrition from multiple algal species in nature.

Project description:The sea slug Plakobranchus ocellatus (Sacoglossa, Gastropoda) retains photosynthetically active chloroplasts from ingested algae (functional kleptoplasts) in the epithelial cells of its digestive gland for up to 10 months. While its feeding behavior has not been observed in natural habitats, two hypotheses have been proposed: 1) adult P. ocellatus uses kleptoplasts to obtain photosynthates and nutritionally behaves as a photoautotroph without replenishing the kleptoplasts; or 2) it behaves as a mixotroph (photoautotroph and herbivorous consumer) and replenishes kleptoplasts continually or periodically. To address the question of which hypothesis is more likely, we examined the source algae for kleptoplasts and temporal changes in kleptoplast composition and nutritional contribution. By characterizing the temporal diversity of P. ocellatus kleptoplasts using rbcL sequences, we found that P. ocellatus harvests kleptoplasts from at least 8 different siphonous green algal species, that kleptoplasts from more than one species are present in each individual sea slug, and that the kleptoplast composition differs temporally. These results suggest that wild P. ocellatus often feed on multiple species of siphonous algae from which they continually obtain fresh chloroplasts. By estimating the trophic position of wild and starved P. ocellatus using the stable nitrogen isotopic composition of amino acids, we showed that despite the abundance of kleptoplasts, their photosynthates do not contribute greatly to the nutrition of wild P. ocellatus, but that kleptoplast photosynthates form a significant source of nutrition for starved sea slugs. The herbivorous nature of wild P. ocellatus is consistent with insights from molecular analyses indicating that kleptoplasts are frequently replenished from ingested algae, leading to the conclusion that natural populations of P. ocellatus do not rely on photosynthesis but mainly on the digestion of ingested algae.

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Seasonality and Longevity of the Functional Chloroplasts Retained by the Sacoglossan Sea Slug Plakobranchus ocellatus van Hasselt, 1824 Inhabiting A Subtropical Back Reef Off Okinawa-jima Island, Japan.

Project description:Plakobranchus ocellatus is a sacoglossan sea slug that feeds on multiple algal species and retains chloroplasts as kleptoplasts for several months. The seasonal differences in the photosynthetic properties of kleptoplasts were examined in sacoglossans collected from a subtropical back reef off of Okinawa-jima (26°21'55"N 127°44'10"E) in 2017-2018. The effective quantum yield of photosystem II in kleptoplasts indicated that stronger ambient light causes more stress in kleptoplasts. The maximum quantum yields (QY) at 20°C, 30°C, and 40°C indicated that kleptoplasts were more functional in photosynthesis in winter than in spring or summer, whereas kleptoplasts may have the highest tolerance to high temperatures in summer. In the long-starvation experiment (LSE), the relative ratio of body weight (relW) linearly decreased and the sacoglossans died within 2 months in the total dark condition, whereas in the LSE with illumination, the animals survived up to 5 months. The time course for the decrease in the relative ratio of the QY (relQY) in the LSE indicated that the photosynthetic function was almost normal for 2 months, regardless of the presence or absence of illumination, after which time relQY gradually decreased to zero. In the field, P. ocellatus continuously took up new kleptoplasts that have suitable properties of photosynthetic ability for each season. In a subtropical environment, in which water temperatures vary from below 20°C to above 30°C, seasonal changes could cause a temporary shortage of algal food and affect the photosynthetic activity of P. ocellatus kleptoplast. Our results, however, indicated the kleptoplasts of P. ocellatus functioned normally for several months and maintained the presence of this sacoglossan in a subtropical environment throughout the year.

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