Comparison of sister species identifies factors underpinning plastid compatibility in green sea slugsProceedings of the Royal Society B: Biological Sciences


J. de Vries, C. Woehle, G. Christa, H. Wagele, A. G. M. Tielens, P. Jahns, S. B. Gould
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Cite this article: de Vries J, Woehle C, Christa

G, Wa¨gele H, Tielens AGM, Jahns P, Gould SB. 2015 Comparison of sister species identifies factors underpinning plastid compatibility in green sea slugs. Proc. R. Soc. B 282: 20142519.

Subject Areas:

Author for correspondence:

Sven B. Gould

Electronic supplementary material is available

Comparison of sister species identifies factors underpinning plastid compatibility sister taxa Elysia cornigera and Elysia timida sequester plastids from the same algal species, but with a very different outcome: while E. cornigera on February 7, 2015 from at or via gould@hhu.decellular biology, physiology, plant science

Keywords: invertebrates, sacoglossa, kleptoplasty, reactive oxygen species, starvation, photosynthetic slugsReceived: 13 October 2014

Accepted: 7 January 2015rspb.royalsocietypublishing.orgusually dies within the first two weeks when deprived of food, E. timida can survive for many months to come. Here we compare the responses of the two slugs to starvation, blocked photosynthesis and light stress. The two species respond differently, but in both starvation is the main denominator that alters global gene expression profiles. The kleptoplasts’ ability to fix CO2 decreases at a similar rate in both slugs during starvation, but only

E. cornigera individuals die in the presence of functional kleptoplasts, concomitant with the accumulation of reactive oxygen species (ROS) in the digestive tract. We show that profiting from the acquisition of robust plastids, and key to E. timida’s longer survival, is determined by an increased starvation tolerance that keeps ROS levels at bay. 1. Introduction

Some sacoglossan slugs can house functional plastids for months in the cytosol of cells that line the animals’ digestive tubules. The slugs steal the plastids (kleptoplasts) from siphonaceous algae upon which they feed. Theory has it that the presence of functional kleptoplasts [1,2] allows some of the sea slug species to survive starvation periods that can last almost a year [3,4]. Recent reports question the categorical importance of photosynthesis during starvation for several species [5,6] and while the animals fix CO2 in a light-dependent manner [5,7– 10], for how long and how much during starvation is not well documented. Animals induce autophagy to reallocate resources through the recycling of tissue when facing starvation [11] and mitochondria-generated reactive oxygen species (ROS) signalling has been found to be a key mediator of autophagy triggered by nutrient deprivation [12,13]. Over the past 20 years, research on ‘photosynthetic (green) slugs’ has focused on understanding how the stolen plastids can remain functional in a foreign cytosol [14], but the molecular response to starvation has not, to our knowledge, been assessed in sacoglossan slugs until now.

The kleptoplasts’ stability outside of the algae disagrees with our knowledge about the sensitivity of land plant plastids, whose photosystem II is highly & 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution

License, which permits unrestricted use, provided the original author and source are green sea slugs

Jan de Vries1, Christian Woehle1, Gregor Christa1, Heike Wa¨gele2,

Aloysius G. M. Tielens3,4, Peter Jahns5 and Sven B. Gould1 1Institute of Molecular Evolution, Heinrich-Heine-University Du¨sseldorf, Universita¨tsstrasse 1, 40225 Du¨sseldorf, Germany 2Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany 3Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine, Utrecht University, Utrecht,

The Netherlands 4Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center,

Rotterdam, The Netherlands 5Plant Biochemistry and Stress Physiology, Heinrich-Heine-University Du¨sseldorf, 40225 Du¨sseldorf, Germany

The only animal cells known that can maintain functional plastids (kleptoplasts) in their cytosol occur in the digestive gland epithelia of sacoglossan slugs. Only a few species of the many hundred known can profit from kleptoplasty during starvation long-term, but why is not understood. The two

Yet, E. cornigera decreased in size more rapidly than

Proc.R.Soc.B 282:20142519 2 on February 7, 2015 from E. timida (figure 1a) and rarely survived more than two weeks without food, which is consistent with previous reports [19,21]. Loss in size was accompanied by a slow fading of the animals’ greenish coloration owing to the loss of the pigments chlorophyll (Chl) b and, most prominently,

Chl a (electronic supplementary material, table S1). In

E. cornigera, pigment concentration declined from starvation day 2 to 4 by 32.9%, but then increased again for a few days in relation to the dry weight of the animals (figure 1b). At day 10, the Chl a and b concentration had dropped from 3109 to 1544 pmol mg21 animal dry weight (49.7%). These values correlate with the rapid decrease observed in body size between day 4 and 7 of starvation (figure 1a). In E. timida, we observed a similar, yet less steep, decline in the concentration of pigments in relation to body mass over the 10 days of starvation measured (from 2193 to 1606 at day 4 (73.2%) and 1638 pmol Chl a þ b/mg animal dry weight at day 10 (74.7%); figure 1b). The increase of photosynthesis-associated pigments around day 6 demonstrates that the animals we measured metabolize their own tissue at an apparently faster rate than the kleptoplasts degrade, which was also observed for starving juveniles of E. chlorotica [23].

Photosynthetic capacity was determined through measurements of photosystem II quantum efficiency (derived from Chlsusceptible to photosynthesis-associated damage [2,15,16].