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.
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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.
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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.
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| 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.
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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.
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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.
References
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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