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Wednesday, May 9, 2012

Endosymbiosis and Photosynthetic Animals

Contributed by: Hong Ma

            Endosymbiosis is thought to be crucial for the early evolution of eukaryotic cells, including the origins of the mitochondrion and the chloroplast, which is essential for photosynthesis. Photosynthesis is generally associated with plants, algae, and bacteria such as cyanobacteria, making these organisms the major primary producers. It is widely accepted that photosynthesis originated in bacteria and that chloroplasts in eukaryotic photosynthetic organisms were derived via ancient endosymbiosis after the capture of a cyanobacterium by an early eukaryote (Fig.1).  This primary endosymbiosis resulted in the ancestor of red algae and green algae. One branch of green algae then evolved into the green plants on land, such as mosses, ferns, and seed plants. The cyanobacterium taken in by the eukaryotic host cell evolved into the organelle chloroplast, which has a greatly reduced genome, whereas most of the original cyanobacterial genes were either lost or transferred into the host nuclear genome. For example, many of the proteins for photosynthesis are now encoded by nuclear genes.
After the origins of red and green algae, secondary symbiotic events (Fig.1) following the capture of one of the red or green algae by other eukaryotes generated a number of highly divergent algae, such as brown algae; however, the origins and histories of many of these algae and other organisms are still uncertain. In these algae, chloroplasts have one or two additional membranes compared with those in red or green algae (and the land plant descendents of green algae), with partial or complete loss of the nuclear genome of the captured red/green algal cells. Because both primary and secondary endosymbioses were both very ancient events, and there are few, if any, intermediate cases, the origin and history of these processes are not well understood.

Fig.1. Diagrams illustrating primary and secondary endosymbiosis. Top: a eukaryotic cell (brown with flagella) takes up a cyanobacterium (blue) and then evolved into red and green algae, as well as glaucophytes (golden algae). Bottom, red algae and green algae are again taken up in secondary endosymbiotic events, one of which gave rise to Vaucheria.

Animals derive nutrients from foods that are ultimately produced by photosynthetic organisms. Lesser known are the amazing symbiotic relationships between members of diverse groups of invertebrates and single-cell photosynthetic algae or bacteria. Such symbiosis is found in sponges, corals, and some giant clams, and provides fixed carbon to the animals, whereas the photosynthetic algae or cyanobacteria also benefit from this relationship in the form of protection and nutrients from the animal partners, such as nitrogen and other minerals. In these mutually beneficial relationships, as much as 90% of the energy needed by the animals can be from the photosynthetic symbionts.
            In the primary and secondary endosynbiotic relationships for plants, algae and other organisms, the ancestral free-living photosynthetic cells had evolved into an organelle, the chloroplast, that depends on the host nuclear genes for biogenesis and function. In addition, chloroplast (or plastid) is maintained throughout the life cycle of plants or algae. In contrast, the relationships between the animal hosts and their photosynthetic symbionts are less intimate, with the symbionts still retaining their cellular structure and complete genomes. Furthermore, the symbiotic relationship is established de novo during animal development. Therefore, the relationships between animals and their symbionts are fundamentally different from those in the primary and secondary endosymbiotic relationships between the plant and algal hosts and their chloroplasts. It is thus difficult to draw inference from the animal – algal symbiotic relationships regarding the evolutionary history of the primary and secondary endosymbioses of the chloroplast.
            Recently, Rumpho et al. (1) described an unusual relationship between a sea slug (Elysia chlorotica) and an alga (Vaucheria litorea). Elysia chlorotica is a green marine animal commonly known as eastern emerald elysia and is found in Eastern US coastal marshes.  It is usually 20-30 mm long, but can grow to as long as 60 mm (Fig. 2). Its food at the juvenile stage is the intertidal Vaucheria litorea, a yellow-green alga and member of the Heterokonts, a diverse group that also includes brown algae. Before feeding on V. litorea, the sea slug has a brown color with red spots and feeding on V. litorea is necessary for the green color.

Fig. 2. Elysia chlorotica, showing highly branched digestive system and green color.

Using an artificial sea-water culture system, Rumpho and coworkers observed that metamorphosis of E. chlorotica from larva to juvenile depends on the presence of V. litorea, and newly formed juvenile starts to feed on the algae immediately. As the sea slug feeds on V. litorea, it breaks the unicellular filamentous alga, and sucks the contents, accumulating chloroplasts in its highly branched digestive system distributed throughout its body. The chloroplasts are taken up by and stored within the cells of the digestive system of the animal in a precess called “kleptoplasty” (Fig. 3), making the body green. The feeding continues until the number of chloroplasts accumulates to a sufficient level, then the sea slug can live as a photosynthetic organism without eating for several months. This ability to use photosynthesis as the sole energy source has endowed the name “solar-powered” sea slug. If, however, the sea slug is removed from the algae within a few days of the start of feeding, then there are insufficient chloroplasts and development arrests.

Fig.3. Kleptoplasty, by which cells of the digestive systems of the sea slug take up chloroplasts from V. litorea, and maintain the function of the chloroplasts.

            Although the V. litorea chloroplasts have four outer membranes, characteristic of such secondary endosymbiotic chloroplasts of heterokonts, the chloroplasts retained in the sea slug seem to lack the two outer membranes. In addition, the V. litorea nuclei or mitochondria were not detected in the sea slug cells, suggesting that only the chloroplasts (without their outer two membranes) are taken up by the cells of the host digestive tract. In other words, the algal nuclei that normally contain the needed gene functions to maintain chloroplast functions appear to be absent in the sea slug cells.
            Therefore, this sea slug –alga relationship is similar to other animal-algal symbiotic relationships in having to establish it de dovo during development, and unlike the endosymbiotic relationship between plants/algae and chloroplasts. However, the E. chlorotica - V. litorea symbiosis is distinct from other animal-algae relationship because the V. litorea chloroplasts are taken up by the E. chlorotica digestive cells, and V. litorea cells are not maintained in the animal. It is striking that during the time when the sea slug is not feeding, even for months, chloroplasts in its digestive cells are functional. One of consequences of the photosynthesis is damage to chloroplast proteins; thus new protein synthesis is needed for the maintenance of chloroplast function. Therefore, the sea slug should be able to provide needed protein activities to repair photo-oxidative damage to chloroplast proteins.
            An attractive hypothesis that explains the ability of E. chlorotica to maintain chloroplast function is that, through repeated uptake of V. litoria cellular content, crucial genes for chloroplast functions have been transferred to the E. chlorotica nuclear genome. Indeed, several lines of evidence support gene transfer from V. litoria to E. chlorotica: de novo protein synthesis of a nuclear-encoded light-harvesting protein, synthesis of the nuclear-encoded PRK protein and light-induced expression of the prk gene in algal-starved sea slugs, and detection of sequences highly similar to V. litoria nuclear genes encoding chloroplast proteins. However, recently a partial transcriptome analysis has failed to identify cDNA sequences that are similar to algal nuclear genes. Nevertheless, the absence of supporting evidence for gene transfer is not evidence for the absence of gene transfer. It is possible that such transferred genes are not expressed highly enough to be detected in the partial transcriptome analysis. Alternatively, the chloroplast functions might be supported via novel mechanisms. Therefore, more extensive and definitive evidence for gene transfer is needed to support the above hypothesis.
            Regardless of the exact mechanisms, E. chlorotica clearly can take up functional chloroplasts intracellularly and maintain their functions for extended periods of several months. These features make this relationship more advanced than other animal-algal symbiotic relationships with intact cellular symbionts and closer to endosymbiotic relationships present in algae. It will be instructive to understand the mechanistic interaction between E. chlorotica and V. litoria and more will be uncovered as much more extensive sequencing efforts are underway. It is possible that in the future, when the soma-germline barrier can be broken for the chloroplast, and when the symbiont chloroplasts can replicate in the sea slug, the relationship will then have evolved into true endosymbiosis.   
1. Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D. 2011. The making of a photosynthetic animal. J. Exp. Biol. 214, 303-311.

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