The Making Of A Photosynthetic Anim

303
The Journal of Experimental Biology 214, 303-311
© 2011. Published by The Company of Biologists Ltd
doi:10.1242/jeb.046540

The making of a photosynthetic animal
Mary E. Rumpho1,*, Karen N. Pelletreau1, Ahmed Moustafa2 and Debashish Bhattacharya3
1

Department of Molecular and Biomedical Sciences, 5735 Hitchner Hall, University of Maine, Orono, ME 04469, USA, 2Department
of Biologyand Graduate Program in Biotechnology, American University in Cairo, New Cairo 11835, Egypt and 3Department of
Ecology, Evolution and Natural Resources, Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08901,
USA
*Author for correspondence (mrumpho@umit.maine.edu)

Accepted 6 August 2010

Summary
Symbiotic animals containing green photobionts challenge thecommon perception that only plants are capable of capturing the
sun’s rays and converting them into biological energy through photoautotrophic CO2 fixation (photosynthesis). ‘Solar-powered’
sacoglossan molluscs, or sea slugs, have taken this type of symbiotic association one step further by solely harboring the
photosynthetic organelle, the plastid (chloroplast). One such sea slug, Elysiachlorotica, lives as a ‘plant’ when provided with
only light and air as a result of acquiring plastids during feeding on its algal prey Vaucheria litorea. The captured plastids
(kleptoplasts) are retained intracellularly in cells lining the digestive diverticula of the sea slug, a phenomenon sometimes referred
to as kleptoplasty. Photosynthesis by the plastids provides E. chlorotica with energy andfixed carbon for its entire lifespan of
~10months. The plastids are not transmitted vertically (i.e. are absent in eggs) and do not undergo division in the sea slug.
However, de novo protein synthesis continues, including plastid- and nuclear-encoded plastid-targeted proteins, despite the
apparent absence of algal nuclei. Here we discuss current data and provide hypotheses to explain howlong-term photosynthetic
activity is maintained by the kleptoplasts. This fascinating ‘green animal’ provides a unique model to study the evolution of
photosynthesis in a multicellular heterotrophic organism.
Supplementary material available online at http://jeb.biologists.org/cgi/content/full/214/2/303/DC1
Key words: Elysia chlorotica, horizontal gene transfer, mollusc, photosynthesis, plastid, seaslug, symbiosis, Vaucheria litorea.

Introduction

It has long been known that photosynthesis takes place in
chlorophyll-containing plants, algae and some bacteria and that it
serves to provide oxygen and energy in the form of biomass to
support heterotrophic life. Some animals (for the purposes of this
review we will address only the metazoans) in the phyla Mollusca
(giant clams,nudibranchs), Porifera (sponges), Cnidaria (corals,
anemones and hydra), Acoelomorpha (flatworms) and Chordata
(ascidians) have evolved mechanisms to capture photosynthetic
products through the formation of symbiotic associations with
intact unicellular algae or cyanobacteria (Fig.1 and supplementary
material TableS1 and references therein). In these cases, the
photobiont (alga orcyanobacterium) acts as an autonomous
photosynthetic factory, providing reduced carbon as a source of
energy to the heterotroph, often receiving nutrients in return.
Whereas initial events leading to primary photosynthetic
eukaryotes involved phagocytosis by a unicellular protist (see
below), the acquisition of photosynthetic symbionts by
multicellular animals poses multiple challenges. Among these are:localization of the symbiont to differentiated tissues, regulation of
the symbiont environment, protein/metabolite transfer and
turnover, evasion or suppression of the host immune response and,
in order for the symbiosis to become permanent, transmission of
the symbiont to the germline (Venn et al., 2008; Raven et al., 2009).
The ability of animals to acquire photobionts appears limited to...