Plastid-bearing Sea Slugs Fix CO2 in the Light but Do Not Require Photosynthesis to Survive

Overview

Journal Proc Biol Sci

Specialty Biology

Date 2013 Nov 22

PMID 24258718

Citations 21

Authors

Gregor Christa

Verena Zimorski

Christian Woehle

Aloysius G M Tielens

Heike Wagele

William F Martin

Sven B Gould

Affiliations

Soon will be listed here.

Abstract

Several sacoglossan sea slugs (Plakobranchoidea) feed upon plastids of large unicellular algae. Four species--called long-term retention (LtR) species--are known to sequester ingested plastids within specialized cells of the digestive gland. There, the stolen plastids (kleptoplasts) remain photosynthetically active for several months, during which time LtR species can survive without additional food uptake. Kleptoplast longevity has long been puzzling, because the slugs do not sequester algal nuclei that could support photosystem maintenance. It is widely assumed that the slugs survive starvation by means of kleptoplast photosynthesis, yet direct evidence to support that view is lacking. We show that two LtR plakobranchids, Elysia timida and Plakobranchus ocellatus, incorporate (14)CO2 into acid-stable products 60- and 64-fold more rapidly in the light than in the dark, respectively. Despite this light-dependent CO2 fixation ability, light is, surprisingly, not essential for the slugs to survive starvation. LtR animals survived several months of starvation (i) in complete darkness and (ii) in the light in the presence of the photosynthesis inhibitor monolinuron, all while not losing weight faster than the control animals. Contrary to current views, sacoglossan kleptoplasts seem to be slowly digested food reserves, not a source of solar power.

Citing Articles

Chromosome-level genome assembly of the sacoglossan sea slug Elysia timida (Risso, 1818).

Manner L, Schell T, Spies J, Galia-Camps C, Baranski D, Ben Hamadou A BMC Genomics. 2024; 25(1):941.

PMID: 39375624 PMC: 11460185. DOI: 10.1186/s12864-024-10829-7.

Kleptoplasty: Getting away with stolen chloroplasts.

Cruz S, Cartaxana P PLoS Biol. 2022; 20(11):e3001857.

PMID: 36346789 PMC: 9642861. DOI: 10.1371/journal.pbio.3001857.

Ultraviolet screening by slug tissue and tight packing of plastids protect photosynthetic sea slugs from photoinhibition.

Havurinne V, Aitokari R, Mattila H, Kapyla V, Tyystjarvi E Photosynth Res. 2021; 152(3):373-387.

PMID: 34826025 PMC: 9458594. DOI: 10.1007/s11120-021-00883-7.

Photosynthesis from stolen chloroplasts can support sea slug reproductive fitness.

Cartaxana P, Rey F, LeKieffre C, Lopes D, Hubas C, Spangenberg J Proc Biol Sci. 2021; 288(1959):20211779.

PMID: 34583582 PMC: 8479339. DOI: 10.1098/rspb.2021.1779.

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

Chihara S, Nakamura T, Hirose E Zool Stud. 2021; 59:e65.

PMID: 34140982 PMC: 8181158. DOI: 10.6620/ZS.2020.59-65.

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