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Photophysiology of kleptoplasts:
photosynthetic use of light by
chloroplasts living in animal cells
João Serôdio1, Sónia Cruz1, Paulo Cartaxana2 and Ricardo Calado1
rstb.royalsocietypublishing.org
Review
Cite this article: Serôdio J, Cruz S, Cartaxana
P, Calado R. 2014 Photophysiology of
kleptoplasts: photosynthetic use of light by
chloroplasts living in animal cells. Phil.
Trans. R. Soc. B 369: 20130242.
http://dx.doi.org/10.1098/rstb.2013.0242
One contribution of 20 to a Theme Issue
‘Changing the light environment: chloroplast
signalling and response mechanisms’.
Subject Areas:
plant science, physiology, cellular biology,
behaviour
Keywords:
kleptoplasty, photoacclimation,
photoprotection, photobehaviour, sacoglossan,
macroalgae
Author for correspondence:
João Serôdio
e-mail: [email protected]
1
Departamento de Biologia and CESAM, Universidade de Aveiro, Campus Universitário de Santiago,
Aveiro 3810-193, Portugal
2
Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Lisboa 1749-016, Portugal
Kleptoplasty is a remarkable type of photosynthetic association, resulting from
the maintenance of functional chloroplasts—the ‘kleptoplasts’—in the tissues
of a non-photosynthetic host. It represents a biologically unique condition
for chloroplast and photosynthesis functioning, occurring in different phylogenetic lineages, namely dinoflagellates, ciliates, foraminiferans and, most
interestingly, a single taxon of metazoans, the sacoglossan sea slugs. In the
case of sea slugs, chloroplasts from macroalgae are often maintained as intracellular organelles in cells of these marine gastropods, structurally intact and
photosynthetically competent for extended periods of time. Kleptoplasty has
long attracted interest owing to the longevity of functional kleptoplasts in
the absence of the original algal nucleus and the limited number of proteins
encoded by the chloroplast genome. This review updates the state-of-the-art
on kleptoplast photophysiology, focusing on the comparative analysis of the
responses to light of the chloroplasts when in their original, macroalgal cells,
and when sequestered in animal cells and functioning as kleptoplasts. It
covers fundamental but ecologically relevant aspects of kleptoplast light
responses, such as the occurrence of photoacclimation in hospite, operation of
photoprotective processes and susceptibility to photoinhibition. Emphasis is
given to host-mediated processes unique to kleptoplastic associations, reviewing current hypotheses on behavioural photoprotection and host-mediated
enhancement of photosynthetic performance, and identifying current gaps
in sacoglossan kleptoplast photophysiology research.
1. Kleptoplasts
Present-day chloroplasts originated from an endosymbiotic process that started
with the acquisition of a photosynthetic ancestral free-living cyanobacterium by
a heterotrophic eukaryote, 1.2 billion years ago [1,2]. Despite this long and intimate coevolution, chloroplasts can be found today living intra-cellularly in
organisms phylogenetically distant from the algal or plant cells in which they
evolved. This is the case for chloroplasts from some macroalgal species that
are ingested by animal herbivores but are not digested along with other cell
components. The organelles resulting from this incomplete digestion, in this
context termed ‘kleptoplasts’, remain structurally intact and photosynthetically competent for long periods, potentially for the entire lifespan of their
new host [3,4]. Kleptoplasty is known to occur in a number of different phylogenetic lineages, such as dinoflagellates, ciliates, foraminiferans and metazoans
[2,5]. The longest studied cases of kleptoplasty are those involving animals, all
marine sacoglossan gastropod molluscs, most within the genus Elysia (figure 1).
These sea slugs feed on macroalgae, either chlorophytes, rhodophytes or
chromophytes, and sequester their chloroplasts in tubule cells of their digestive
epithelium [3,6]. Despite the very small number of species known to participate in kleptoplasty, kleptoplastic organisms are not rare, and may even be
cosmopolitan and form large populations, thus denoting a successful and
well-adapted life form.
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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(b)
(c)
(d)
2
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(a)
Kleptoplasty has raised considerable interest owing to the
longevity of functional kleptoplasts in the absence of the original algal nucleus. In algae and plants, the processes required
for chloroplasts to function are known to depend heavily on
the continuous production, repair and replacement of plastid
components, such as pigments, proteins and enzymes [7,8].
These processes involve intercompartmental crosstalk between the plastid and the nucleus, through both anterograde
(nucleus-to-plastid) and retrograde ( plastid-to-nucleus) signalling [9]. Furthermore, many of the photosynthetic proteins and
enzymes required for general maintenance of the photosynthetic apparatus are nuclear-encoded and targeted to the
chloroplast, with the expression of plastid-encoded genes
also regulated by nuclear-encoded proteins [10]. Additionally,
most of the metabolic machinery that equipped the ancestral
cyanobacterium progenitor from which chloroplasts descended was lost during evolution inside their eukaryotic host,
together with a large part of the original genome, which was
transferred to the nucleus of the heterotrophic host cell [11]. Ironically, it is this ‘incomplete’ photosynthetic plastid that finds
itself inside a new, unfamiliar host, for which evolution has
not prepared it for—rather on the contrary. Modern chloroplasts may thus be expected to be largely unable to lead an
autonomous life without the cell nucleus, making kleptoplasty
in animal cells particularly intriguing as plastids and animal
cells are phylogenetically unrelated and the latter were never
photosynthetic [1].
Crosstalk between organelles is particularly important in
the case of the chloroplast and nucleus, as frequent changes
in the light environment require a continuous regulation
of responses to maintain optimal photosynthetic function
[10,12]. These include a range of processes involving shortand long-term photoacclimation and the efficient operation
of photoprotective mechanisms against photoinhibition.
Here, we intend to update the state-of-the-art on kleptoplast photophysiology, centred on the comparative analysis
of light responses of chloroplasts in their original macroalgal
cells and when functioning as kleptoplasts, with emphasis on
metazoan host-mediated processes affecting light exposure
and photosynthetic performance.
2. Photoacclimation
Responses to changes in light environment primarily involve
photoacclimation, phenotypic adjustments in various components of the photosynthetic apparatus to regulate excitation
pressure, and maintaining carbon fixation while avoiding
photo-oxidative stress. In eukaryotic algae, photoacclimation
includes a range of processes such as changes in cellular content
of photosynthetic reaction centres (RCI and RCII), photosynthetic and photoprotective pigments, photosynthetic unit
number and size, photosystem II (PSII)/photosystem I stoichiometry, as well as protein degradation and de novo protein
synthesis that regulate the amount of antennae proteins and
the content and activity of RuBisCO and other enzymes [12].
The question of whether kleptoplasts are able to undergo
photoacclimation in hospite is particularly relevant because several of the processes involved in photoacclimation require
extensive expression of nuclear-encoded genes [2,4]. At present,
available evidence is still based on a small number of associations
but does not indicate the occurrence of photoacclimation in
Phil. Trans. R. Soc. B 369: 20130242
Figure 1. The kleptoplast-bearing sacoglossan sea slugs (a) Elysia viridis, feeding on Codium tomentosum, and (b) Elysia chlorotica, feeding on Vaucheria litorea, and
showing the opened parapodia (c,d, respectively). Courtesy of C. Brandão (a), A. Kharlamov (c), M. E. Rumpho and K. N. Pelletreau (b,d ).
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kleptoplasts (sea slug)
(a)
3
1.2
1.0
0.8
0.6
0.4
a
y = 1.04x – 0.15
r2 = 0.846**
0.2
kleptoplasts (sea slug)
0.2
0.4
0.6
0.8
1.0
1.2
150
100
50
0
(c) 1000
rETRm
y = 1.20x + 14.82
r2 = 0.835*
50
100
150
200
800
600
400
200
0
Ek
y = 1.86x + 26.24
r2 = 0.844*
100 200 300 400
chloroplasts (algae)
500
E. viridis/C. fragile [13]
E. timida/A. acetabulum [15]
E. timida/A. acetabulum [16]
T. hopei/unidentified algae [17]
E. viridis/C. tomentosum (July)
E. viridis/C. tomentosum (November)
3. Host-mediated enhanced photosynthetic
performance
Figure 2. Linear relationship between published LC parameters (a) a, (b)
rETRm and (c) Ek measured in chloroplasts (intact algae) and corresponding
kleptoplasts (inside the animal host). Elysia viridis and E. timida are longterm retention species (functional kleptoplasts for more than 8 days),
whereas Thuridilla hopei is a short-term retention species (kleptoplasts functional up to 8 days) [17]. The data for E. viridis/C. fragile [13] are the average
of the values measured after the sea slugs filled their digestive cells with
functional chloroplasts. Dotted lines indicate the 1 : 1 ratio. Specimens collected as in Cruz et al. [18], in July and November 2012. LCs measured
and parameters estimated following Vieira et al. [14].
Since its beginning, research on kleptoplast photosynthesis has
predominantly focused on the provision of photosynthates to
the host [24–26]. It seems that host animals receive a clear
benefit from harbouring kleptoplasts, by obtaining a significant amount of carbon from photosynthesis (up to 60% of the
carbon input was estimated to be derived from kleptoplast
photosynthesis, for the Oxynoe viridis/Caulerpa longifolia
association [25]). Furthermore, the assimilation of nitrogen
was seen to be mediated by kleptoplasts, for E. viridis/
C. fragile [27]. However, evidence is accumulating that the
kleptoplastic association may also be transiently beneficial
for the functioning of the sequestered plastid, despite their
shortened lifespan. In fact, a number of recent studies have
shown that the photosynthetic performance of kleptoplasts
appears to be superior to corresponding chloroplasts within
their original algal cells [13,15,16]. This agrees with the recognition that many non-photosynthetic hosts are able to
enhance the photosynthetic release of non-kleptoplastic
Phil. Trans. R. Soc. B 369: 20130242
0
(b) 200
kleptoplasts (sea slug)
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kleptoplasts. For the association Elysia viridis/Codium fragile, no
differences in pigment content (normalized to chlorophyll a)
were found between host and algal prey collected from the
wild [13]. Also, for the case of E. viridis/Codium tomentosum,
no changes in light-response curves (LC) of photosynthetic
activity consistent with photoacclimation were observed when
recently collected kleptoplast-bearing individuals were exposed
to contrasting light regimes [14].
The absence of photoacclimation in kleptoplasts is also
consistent with the strong association between LCs of relative
electron transport rate (rETR) of algal food and corresponding
kleptoplastic hosts. A compilation of all published results
[13,15–17] and original data (S. Cruz, T. Santos, P. Cartaxana,
R. Calado, J. Serôdio, unpublished; http://dx.doi.org/10.
6084/m9.figshare.783888) showed that despite the large
range in algal prey photoacclimation state (as denoted by the
light-response curve photoacclimation parameter Ek, ranging
from 28.7 to 356.0 mmol m22 s21), LC parameters of the macroalgae and kleptoplasts in their animal host cells were
significantly correlated (figure 2). Significant correlations
were found for parameters related to light-limited (a, given
by the initial slope of the LC; figure 2a) and light-saturated
photosynthesis (rETRm, the maximum rETR reached in the
LC, figure 2b) as well as for Ek (figure 2c), indicating that a significant proportion of the variability of the light response of the
kleptoplasts could be explained by the light response of the
macroalgae’s chloroplasts. The lowest Ek values were found
for E. viridis and C. tomentosum, consistent with the low-light
environment inside the macroalgae’s dark fronds. By contrast,
the highest Ek values were found for the light and optically thin
Acetabularia acetabulum and its herbivore Elysia timida.
The association found between the LCs of the host and its
algal food shown in this meta-analysis suggests that the kleptoplast may not undergo significant photoacclimation and that
the kleptoplastic host’s photoacclimation state essentially
reflects the light environment of the ingested chloroplasts
while inside the algal tissues. The absence of photoacclimation
in kleptoplasts is consistent with their inability to synthesize
crucial photosynthetic pigments, for example chlorophyll a,
reported for various kleptoplastic associations [13,19]. However, in the case of Elysia chlorotica/Vaucheria litorea, and
Elysia clarki/unidentified macroalgal species, kleptoplasts
were shown to be capable of synthesizing chlorophylls and
some chloroplast proteins [20–23]. While this remarkable
capacity is likely to be relevant for the repair and replacement
of pigments and proteins required for prolonging the functional status of kleptoplasts, it is uncertain whether this is
enough to support changes in the photoacclimation state.
60
50
Elysia
40
30
Elysia-inherent
20
Codium
10
0
200
400
600
800
irradiance (µmol m–2 s–1)
1000
Figure 3. Host-mediated increase in photosynthetic performance in the association E. viridis/C. tomentosum and effects of depth integration of subsurface
fluorescence. LCs of rETR as measured in intact (depth-integration effects present)
E. viridis (‘Elysia’) and C. tomentosum (‘Codium’), and on corresponding optically
thin samples (depth-integration effects minimized), E. viridis individuals placed in
a 0.5 mm deep concavity microscope slide and covered by a coverslip, and a slurry
of C. tomentosum (‘Elysia-inherent’ and ‘Codium-inherent’, respectively). Mean
values of five replicates. Vertical bars represent 1 s.d. Specimens collected as
in Cruz et al. [18]. LCs measured following Vieira et al. [14].
endosymbionts [5]. This tendency is also evident when analysing available datasets comparing fluorescence LC parameters
measured in the host and the algae, summarized in figure 2.
While no marked differences were found for light-limited
photosynthesis (a; regression slope 1; figure 2a), most
rETRm values (with the exception of Thuridilla hopei/unidentified algae) were significantly higher for the kleptoplast-bearing
host than for the algal prey (slope . 1; figure 2b), supporting
that the host somehow favours light-saturated photosynthesis
of sequestered plastids.
In this context, it is important to note that the direct comparison of fluorescence data measured on sea slugs and macroalgae
must be interpreted carefully. This is because fluorescence LCs
measured on samples with such markedly different optical
properties may be strongly affected by artefactual effects causing the overestimation of LC parameters independently of the
inherent photophysiological response [28]. Depth-integration
effects are illustrated in figure 3, comparing LCs measured on
E. viridis and C. tomentosum when they are present (undisturbed
specimens) and when they are minimized (‘inherent’ light
response; macroalgae slurry and sea slug compressed in a thin
concavity microscope slide). rETRm was found to reach considerably higher values (80.2%) for the sea slugs than for
macroalgae. Of comparable relevance was the overestimation
due to optical effects, with optically thin samples (i.e. inherent)
displaying rETRm values of 32.7% and 27.5% lower for the
macroalga and the sea slug, respectively.
Higher photosynthetic performance of kleptoplasts has
been tentatively attributed to their increased light exposure
along the highly branched digestive gland of sacoglossan
sea slugs [13] or to improved photoprotection provided by
a combination of xanthophyll cycle operation and host behaviour [15]. Nonetheless, these hypotheses seem problematic:
in the first case, because an increase in light availability can
be expected to affect light-limited photosynthesis, but not,
by definition, light-saturated photosynthetic rates; in the
second case, because the activation of the xanthophyll cycle
4. Photoprotection and photoinhibition
Photoprotective mechanisms are necessary to deal with light
energy absorbed in excess of that used by photochemical
pathways and carbon fixation [29,30]. They are crucial in preventing the accumulation of reactive oxygen intermediates
and minimizing photodamage to the photosynthetic apparatus [7]. For kleptoplasts, efficient photoprotection can be
expected to be of major importance. On the one hand, plastids may be exposed to a new light environment, because
of differing light attenuation properties of the host’s tissues
and its active motility in high light habitats, to which they
may not be acclimated. On the other hand, damage caused
by inefficient photoprotection may be harder to overcome
and even aggravated in the absence of a fully functional
PSII protein repair system. Recovery from photoinhibition
relies heavily on repair and de novo synthesis of PSII proteins,
for example the subunit D1, as damage from reactive oxygen
species (ROS) occurs not only through direct inactivation of
the PSII proteins, but mostly by inhibiting the repair of
photodamaged components [7]. While synthesis of D1 and
other PSII proteins were observed in kleptoplasts of the
E. chlorotica/V. litorea association [21], this outstanding
capacity does not seem to be widespread. For E. viridis/
C. tomentosum, exposure to moderate light levels of only
140 mmol m22 s21 were found to cause a major decrease in
kleptoplast longevity (on average, from 30.8 to 10.2 days), consistent with light dose-dependent photoinhibition [14]. Despite
its importance, little is known on the operation of photoprotective mechanisms in kleptoplasts (reviewed in [28]). The
4
Phil. Trans. R. Soc. B 369: 20130242
Codium-inherent
requires exposures to excess light in the time scale of tens
of minutes [29,30], being thus largely irrelevant to explain
changes in fluorescence LCs, as these record instantaneous
photosynthetic activity, and during which actual exposure
to high light is too short. On the other hand, no experimental
evidence has thus far been provided to support that behavioural responses to high light have a photoprotective value
(see below).
An alternative explanation for the enhanced photosynthetic
performance of kleptoplasts is the likely intra-cellular supply
of respired inorganic carbon and nutrients produced by the
metabolism of the host. The importance of inorganic carbon
and nutrient translocation from the heterotrophic host to the
photosynthetic endosymbiont is well established in other
marine animal–alga symbiotic associations, namely those
between corals and dinoflagellates [31]. Enhancing effects on
kleptoplast photosynthesis may thus be expected to occur in
marine environments where inorganic carbon and nutrient
availability is often limiting for algal photosynthesis [6]. This
hypothesis is consistent with the observation that light-saturated
(rETRm), not light-limited (a), photosynthesis shows the greatest
increase in the kleptoplastic host, presumably owing to an insufficient supply of inorganic carbon, which is a main limiting
factor of photosynthesis under light saturation. Another way
the animal intra-cellular environment may enhance photosynthesis is through the inhibition of photorespiration. As the
intensity of photorespiration depends on the CO2 to O2 ratio at
the RuBisCO site [32], a decrease in photorespiration in kleptoplasts may be expected not only because more CO2 is made
available but also owing to the higher consumption of O2 in
the host animal cell through respiration.
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relative electron transport rate (rETR)
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5. Host-mediated photoprotection?
6. Currents gaps: oxidative stress and reactive
oxygen species signalling
Kleptoplasty is an exciting research topic, as it represents a naturally occurring biologically unique condition for chloroplast
and photosynthesis functioning. While the first studies on
Acknowledgements. We thank Mary E. Rumpho and Karen N. Pelletreau,
Cláudio Brandão and Alexander Kharlamov for photographs of sacoglossa. We thank Tânia Santos for help in field and laboratory work.
We thank two anonymous reviewers for their comments on the
manuscript.
Funding statement. This work was supported by the Fundação para
a Ciência e a Tecnologia, through grant no. SFRH/BPD/74531/
2010 and by the FP7 Marie Curie Career Integration grant no.
PCIG11-GA-2012-322349 (S.C.).
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