Elysia Chlorotica - The Solar Powered Sea Slug

Elysia chlorotica (commonly known as the eastern emerald elysia) is a petite to moderately sized species of green sea slug, a marine opisthobranch gastropod mollusk. This sea slug bears a resemblance to nudibranchs, although it doesn't fall within that clade. Instead, it belongs to the Sacoglossa clade, a group of sap-sucking sea slugs. Some members of this clade incorporate chloroplasts from the algae they consume for photosynthesis, a phenomenon referred to as . Elysia chlorotica stands as one example of these "solar-powered sea slugs" and forms a subcellular endosymbiotic relationship with chloroplasts from the marine heterokont alga Vaucheria litorea.

Eastern emerald elysia

( Elysia chlorotica )

Image by Patrick J. Krug,CC BY-NC 3.0,via Wikimedia Commons 

Scientific classification
Kingdom	Animalia
Phylum:	Mollusca
Class:	Gastropoda
Subclass:	Heterobranchia
Family:	Plakobranchidae
Genus:	Elysia
Species:	E. chlorotica

Elysia chlorotica (commonly known as the eastern emerald elysia) is a petite to moderately sized species of green sea slug, a marine opisthobranch gastropod mollusk. This sea slug bears a resemblance to nudibranchs, although it doesn't fall within that clade. Instead, it belongs to the Sacoglossa clade, a group of sap-sucking sea slugs. Some members of this clade incorporate chloroplasts from the algae they consume for photosynthesis, a phenomenon referred to as kleptoplasty.

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Kleptoplasty

Kleptoplasty or kleptoplastidy is a phenomenon in symbiotic connections where plastids, particularly chloroplasts sourced from algae, are assimilated by the host. The term originates from Kleptes (κλέπτης), the Greek word for thief. The algae are consumed in a typical manner, undergoing partial digestion while leaving the plastid unharmed. These plastids persist within the host, temporarily sustaining photosynthesis and conferring benefits to the host organism. The concept of kleptoplasty was coined in 1990 to elucidate chloroplast symbiosis.

Elysia chlorotica stands as one example of these "solar-powered sea slugs" and forms a subcellular endosymbiotic relationship with chloroplasts from the marine heterokont alga Vaucheria litorea.

Adults typically displays a vibrant green hue due to the presence of Vaucheria litorea chloroplasts in the cells of the slug's digestive diverticula. Lacking a protective shell or other defense mechanisms, the green color acquired from the algae serves as effective camouflage against predators. By assimilating the green hue from the chloroplasts, the slugs seamlessly blend with the sea bed, enhancing their chances of survival and overall fitness. On occasion, they may exhibit reddish or greyish tones, believed to be influenced by the chlorophyll content in the branches of the digestive gland throughout the body. This species may also feature minute red or white spots scattered across the body. Juveniles, before feeding on algae, sport a brown color with red pigment spots due to the absence of chloroplasts. Elysia chlorotica possesses a characteristic elysiid shape, characterized by large lateral parapodia that can fold over to enclose the body. While capable of growing up to 60 mm in length, they are more commonly found in the 20 mm to 30 mm range.

Distribution and Habitat

Range map of Elysia chlorotica from iNaturalist.org, CC BY-NC 4.0.

Elysia chlorotica inhabits the eastern shores of the United States, encompassing states like Massachusetts, Connecticut, New York, New Jersey, Maryland, Rhode Island, Florida (both east and west regions), and Texas. Its presence extends as far north as Nova Scotia, Canada. This species predominantly thrives in salt marshes, tidal marshes, pools, and shallow creeks, occupying depths ranging from 0 m to 0.5 m.

Feeding

A defined tubule of the digestive diverticula extending into the parapodial region of the animal (arrow) by Karen N. Pelletreau et al. via Wikimedia commons

Elysia chlorotica feeds on intertidal alga Vaucheria litorea, puncturing its cell wall with a radula. It retains only chloroplasts, storing them in its digestive system, and incorporates live chloroplasts into its gut cells, maintaining them for months. The acquisition of chloroplasts begins after metamorphosis, with juvenile slugs turning green after feeding on algae due to chloroplast distribution in the extensively branched gut. Initially relying on a continuous intake of algae, over time, chloroplasts stably incorporate into gut cells, enabling the slug to remain green without further feeding. Some Elysia chlorotica slugs can use photosynthesis for up to a year after minimal feedings.

The algae's chloroplasts become integrated into the cell via phagocytosis, a process where sea slug cells engulf algae cells, incorporating chloroplasts into their own cellular structure. Elysia chlorotica utilizes the incorporated chloroplasts to harness energy directly from light through photosynthesis, akin to most plants. During periods of limited algae as a food source, E. chlorotica can endure for months. Initially, it was believed survival relied on sugars produced by chloroplasts through photosynthesis; however, research indicates chloroplasts can endure and function for up to nine or even ten months.

Nevertheless, additional research on various analogous species revealed that these marine mollusks thrive equally well in the absence of light. Sven Gould and his colleagues from Heinrich-Heine University in Düsseldorf demonstrated that, even with photosynthesis hindered, the slugs could endure prolonged periods without food, showing comparable resilience to light-exposed, food-deprived counterparts. The team subjected six P. ocellatus specimens to a 55-day starvation experiment, placing two in darkness, treating two with photosynthesis-inhibiting chemicals, and exposing two to appropriate light. Surprisingly, all specimens survived, exhibiting similar weight loss rates. In a similar trial with six E. timida specimens denied food and kept in complete darkness for 88 days, all specimens emerged unscathed.

In a different study, it was demonstrated that E. chlorotica indeed possess a mechanism to sustain the viability of their chloroplasts. Following an eight-month duration, despite the Elysia chlorotica appearing less verdant and more yellowish, a significant portion of the chloroplasts within the slugs seemed to have remained undamaged while preserving their delicate structure. By redirecting less energy to tasks like foraging for food, the slugs can prioritize crucial activities. Although Elysia chlorotica cannot produce their own chloroplasts, the capacity to uphold chloroplasts in a functional state suggests that Elysia chlorotica may harbor photosynthesis-supporting genes within their nuclear genome, potentially acquired through horizontal gene transfer. As chloroplast DNA alone encodes merely 10% of the proteins essential for effective photosynthesis, scientists explored the Elysia chlorotica genome for potential genes supporting chloroplast survival and photosynthesis. The researchers identified a crucial algal gene, psbO (a nuclear gene encoding a manganese-stabilizing protein within the photosystem II complex) in the sea slug's DNA, identical to the algal counterpart.

They inferred that the gene likely underwent horizontal gene transfer, as it was already present in the eggs and sex cells of Elysia chlorotica. It is this capacity for horizontal gene transfer that enables the chloroplasts to be utilized as efficiently as observed. If an organism failed to assimilate the chloroplasts and associated genes into its cells and genome, algal cells would require more frequent consumption due to inefficiencies in utilizing and preserving chloroplasts. This, contributes to energy conservation, allowing the slugs to prioritize crucial activities like mating and evading predation.

More recent analyses, however, failed to pinpoint actively expressed algal nuclear genes in Elysia chlorotica, as well as in the analogous species Elysia timida and Plakobranchus ocellatus. These findings undermine support for the horizontal gene transfer hypothesis. A 2014 study using fluorescent in situ hybridization (FISH) to locate an algal nuclear gene, prk, uncovered signs of horizontal gene transfer. Nevertheless, these results have been contested, as FISH analysis can be misleading and cannot substantiate horizontal gene transfer without comparing to the Elysia chlorotica genome, a step overlooked by the researchers.

The exact mechanism that maintains chloroplast longevity in Elysia chlorotica after capture, despite the absence of active algal nuclear genes, remains unknown. Nonetheless, some insight has been gained into Elysia timida and its algal sustenance. Genomic analysis of Acetabularia acetabulum and Vaucheria litorea, the primary food sources for Elysia timida, has disclosed that their chloroplasts produce ftsH, another essential protein for photosystem II repair. While in land plants this gene is invariably encoded in the nucleus, it is present in the chloroplasts of most algae. An abundant supply of ftsH could, in theory, significantly contribute to the observed kleptoplast longevity in Elysia chlorotica and Elysia timida. 

Life-Cycle

Adult Elysia chlorotica exhibit simultaneous hermaphroditism, producing both sperm and eggs concurrently. While self-fertilization is infrequent in this species, cross-copulation is the preferred method. Once fertilization occurs internally within the slug, Elysia chlorotica deposit their fertilized eggs in elongated strings.

Cleavage

Within the life cycle of Elysia chlorotica, holoblastic and spiral cleavage takes place. This entails complete cleavage of the eggs, and each cleavage plane occurs at an oblique angle to the animal-vegetal axis of the egg. Consequently, tiers of cells are generated, with each tier situated in the furrows between cells of the tier below. Culminating in a stereoblastula, the embryo forms a blastula

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Blastula

The blastula (derived from Greek βλαστός (blastos meaning bud)) is a spherical arrangement of cells referred to as blastomeres encircling an internal fluid-filled space known as the blastocoel. Embryonic development initiates with a sperm fertilizing an egg cell to give rise to a zygote, which undergoes numerous cleavages to evolve into a cluster of cells termed a morula. Only upon the formation of the blastocoel does the early embryo transform into a blastula. The blastula precedes the emergence of the gastrula where the germ layers of the embryo take shape.

without a distinct central cavity.

Gastrulation

Gastrulation in Elysia chlorotica follows an epibolic process: the ectoderm

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Ectoderm

The ectoderm is one of the three fundamental germ layers established during early embryonic development. It constitutes the outermost layer, positioned above the mesoderm (the intermediary layer) and endoderm (the innermost layer). This layer arises and stems from the outermost stratum of germ cells. The term ectoderm derives from the Greek ektos, signifying "external," and derma, signifying "tissue."

extends to encompass the mesoderm

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Mesoderm

The mesoderm serves as the central stratum among the trio of germ layers emerging in gastrulation during the early stages of embryo development in most animals. The exterior layer is the ectoderm, while the internal layer is the endoderm.

The mesoderm gives rise to mesenchyme, mesothelium, non-epithelial blood cells, and coelomocytes. Mesothelium encases coeloms. Mesoderm orchestrates the formation of muscles through myogenesis, septa (cross-wise partitions), and mesenteries (length-wise partitions); it also contributes to the composition of gonads, with the remainder being gametes. Myogenesis is specifically associated with the function of mesenchyme.

and endoderm.

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Endoderm

Endoderm, the deepest of the three primary embryonic germ layers, plays a central role in early embryo development. The remaining layers include ectoderm (outer layer) and mesoderm (intermediate layer). Cells moving inward through the archenteron shape the gastrula's inner layer, ultimately giving rise to the endoderm. Initially composed of flattened cells, the endoderm later transforms into columnar cells, forming the epithelial lining of various systems.

Larval stage

Following a trochophore-like stage in development, the embryo hatches into a veliger larva. This larva possesses a shell and a ciliated velum, which it employs for swimming and transporting food to its mouth. Feeding on phytoplankton in the sea-water column, the veliger larva uses its ciliated velum to convey food to the mouth. Subsequently, the food undergoes sorting in the stomach before progressing to the digestive gland, where digestion occurs, and nutrients are absorbed by the epithelial cells of the digestive gland.

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References

• Wägele H, Deusch O, Händeler K, Martin R, Schmitt V, Christa G, et al. (2011). "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". Mol Biol Evol. 28 (1): 699–706. doi:10.1093/molbev/msq239. PMC 3002249. PMID 20829345. Retrieved on November 6, 2023, from
  https://www.researchgate.net/profile/Sven-Gould/publication/46191434_Transcriptomic_Evidence_That...-Elysia-timida-and-Plakobranchus-ocellatus-Does-Not-Entail-Lateral-Transfer-of-Algal-Nuclear-Genes.pdf.
   

• Christa G, de Vries J, Jahns P, Gould SB (2014). "Switching off photosynthesis: the dark side of sacoglossan slugs". Communicative & Integrative Biology. 7 (1): e28029. doi:10.4161/cib.28029. PMC 3995730. PMID 24778762. Retrived on November 30, 2023, from
https://www.researchgate.net/profile/Sven-Gould/publication/258824182_Plastid-bearing_sea_slugs_fix_CO2_in_the_light_but_do_not_require_photosynthesis_to_survive/links/02e7e52920d33e1d3d000000/Plastid..._tp=eyJjb250ZXh0Ijp7ImZpcnN0UGFnZSI6InB1YmxpY2F0aW9uIiwicGFnZSI6InB1YmxpY2F0aW9uIn19.

 

• Rumpho ME, Worful JM, Lee J, et al. (November 2008). "Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica". Proc. Natl. Acad. Sci. U.S.A. 105 (46): 17867–17871. doi:10.1073/pnas.0804968105. PMC 2584685. PMID 19004808. Retrived on November 30, 2023, from
https://www.researchgate.net/profile/James-Manhart/publication/23469250_Horizontal_gene_transfer_of_the_algal_nuclear_gene_psbO_to_..._tp=eyJjb250ZXh0Ijp7ImZpcnN0UGFnZSI6InB1YmxpY2F0aW9uIiwicGFnZSI6InB1YmxpY2F0aW9uIn19.

   

• Christa G, Zimorski V, Woehle C, Tielens AG, Wägele H, Martin WF, Gould SB (2013). "Pastid-bearing sea slugs fix CO2 in the light but do not require photosynthesis to survive". Proceedings of the Royal Society B. 281 (1774): 20132493. doi:10.1098/rspb.2013.2493. PMC 3843837. PMID 24258718. Retrived on November 30, 2023, from
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• de Vries J, Habicht J, Woehle C, Huang C, Christa G, Wägele H, et al. (2013). "Is ftsH the key to plastid longevity in sacoglossan slugs?". Genome Biol Evol. 5 (12): 2540–8. doi:10.1093/gbe/evt205. PMC 3879987. PMID 24336424. Retrived on November 30, 2023, from
https://scholar.google.com/scholar_url?url=https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2013.2493%3Fdownload%3Dtrue&hl=en&sa=T&oi=ucasa&ct=ufr&ei=qVhxZf6PJYu5ywSnupvoBg&scisig=AFWwaebrib2qFK43-zIRLV8rW9qC.

   

• Rumpho-Kennedy, M.E., Tyler, M., Dastoor, F.P., Worful, J., Kozlowski, R., & Tyler, M. (2006). Symbio: a look into the life of a solar-powered sea slug. Retrived on November 30, 2023, from
https://doi.org/10.1104/pp.123.1.29.

   

• "Solar-Powered Slugs Are Not Solar-Powered". National Geographic. Retrived on November 30, 2023, from
https://www.nationalgeographic.com/science/article/solar-powered-slugs-are-not-solar-powered...concluded%20that%20the,need%20to%20photosynthesise%20to%20survive..