Lipidomics of solar-power animals: a tool to unravel the process of kleptoplasty
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1
Department of Biology, University of Aveiro, Portugal
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2
Department of Chemistry, University of Aveiro, Portugal
Marine environments are a surprise box where it is possible to find astonishing associations, such as solar-powered animals. Although photosynthesis and animals are two apparently incompatible terms, both merge in sacoglossan sea slugs. This animal group is the only metazoan known to retain functional chloroplasts from its macroalgal food (Rey et al., 2017). These sea slugs are very selective feeders, choosing their food items from a small group of macroalgae. During feeding, these sea slugs use their radula to penetrate the cell wall of siphonaceous algae and suck the entire cytosolic content. The whole algal content is digested except for chloroplasts, which are phagocytized into the digestive epithelium. These stolen chloroplasts (kleptoplasts) remain intact and photosynthetically active inside the animal cells for different periods of time, from only a few hours to several months, depending on the sea slug species. While the mechanisms and functions of kleptoplasty are still poorly understood, there are growing experimental evidences that kleptoplasts provide an additional source of energy to sacoglossan sea slugs (Cartaxana et al., 2017).
Chloroplast envelop membranes are lipid-rich structures, where glycerolipids (galactolipids, phospholipids, sulfolipids) represent the bulk matrix maintaining membrane architecture and, together with pigments, represent the essential elements to perform photosynthesis (Block et al., 2007). The lipidome profile of chloroplast membranes includes glycolipids (e.g. galactolipids, sulfolipids), exclusive lipids of chloroplast membranes.
The objective of the present study was to identify potential shifts in the lipidome of macroalgal chloroplasts sequestered by sacoglossan sea slug species with different retention times of kleptoplasty.
Elysia viridis and Placida dendritica are two two autochthonous species of the Portuguese coast, with high and low retention time of kleptoplasty, respectively. The natural habitat of both species is the green macroalga Codium tomentosum, where both species inhabit. Sea slug species were surveyed at two different periods: immediately after being collected from the field and after one-week of starvation in captivity. A lipidomic mass spectrometry-based analysis was performed to study the exclusive lipids from chloroplast membranes in C. tomentosum, E. viridis and P. dendritica, using hydrophilic interaction liquid chromatography-mass spectrometry (HILIC-LC-MS) and MS/MS.
The lipidomic analysis of sea slugs collected in the field revealed that the most abundant molecular species of galactolipids (MGDG, MGMG, DGDG, DGMG) identified in C. tomentosum were also present in both sea slug species, although in lower concentrations. The total number of galactolipid molecular species identified in P. dendritica was lower than in E. viridis, which was lower than in C. tomentosum. After one-week of starvation, there was a general decrease in the relative abundance of several molecular species. In P. dendritica all molecular species presented a significant lower relative abundance, or even disappeared during starvation. This finding confirmed the loss of photosynthetic activity by stolen plastids. On the other side, in E. viridis, this reduction was less marked, with the lyso-forms of galactolipids (MGMG, DGMG) increasing under starvation (likely related to the activity of galactolipases during this stressful period). Regarding sulfolipids (SQDG, SQMG), the lipidome of E. viridis was very similar to that of C. tomentosum, indicating a preservation of photosynthetic activity in kleptoplasts. These results confirm that an earlier degradation occurs in the chloroplast membranes of P. dendritica, when compared to E. viridis. Moreover, a remodeling of kleptoplast membranes during starvation in E. viridis is also likely to occur.
Figure caption
Figure 1 Schematic representation of the methodology used in the lipidomic mass- spectrometry analysis of the macroalga Codium tomentosum and the sacoglossan sea slugs Elysia viridis and Placida dendritica.
Figure 2 a) Number of molecular species of galactolipids (MGDG, MGMG, DGDG, DGMG) and sulfolipids (SQDG, SQMG) identified in the macroalga Codium tomentosum and the sacoglossan sea slugs Elysia viridis and Placida dendritica. Both sacoglossan sea slug species were surveyed immediately after being collected from the field and after one-week of starvation in captivity. b) Relative abundance of MGDG, DGDG and SQDG molecular species identified in E. viridis and P. dendritica immediately after being collected from the field and after one-week of starvation in captivity.
Acknowledgements
Felisa Rey (SFRH/BPD/115347/2016) is grateful to FCT, POCH and ESF. The present study was funded by FEDER through COMPETE (POCI-01-0145-FEDER-016754), by National funding through FCT (PTDC/BIA-ANM/4622/2014). Thanks are due for the financial support to CESAM (UID/AMB/50017/2019), to FCT/MCTES through national funds, for the financial support to QOPNA & LAQV/REQUIMTE (FCT UID/QUI/00062/2019), to the Portuguese Mass Spectrometry Network (LISBOA-01-0145-FEDER-402-022125).
References
Block, M. A., Douce, R., Joyard, J., and Rolland, N. (2007). Chloroplast envelope membranes: A dynamic interface between plastids and the cytosol. Photosynth. Res. 92, 225–244. doi:10.1007/s11120-007-9195-8.
Cartaxana, P., Trampe, E., Kühl, M., Cruz, S., Dionísio, G., Faleiro, F., et al. (2017). Kleptoplast photosynthesis is nutritionally relevant in the sea slug Elysia viridis. Sci. Rep. 7, 7714. doi:10.1038/s41598-017-08002-0.
Rey, F., Costa, E. da, Campos, A. M., Cartaxana, P., Maciel, E., Domingues, P., et al. (2017). Kleptoplasty does not promote major shifts in the lipidome of macroalgal chloroplasts sequestered by the sacoglossan sea slug Elysia viridis. Sci. Rep. 7, 11502. doi:10.1038/s41598-017-12008-z.
Keywords:
Chloroplasts,
Codium tomentosum,
Glycolipids,
Mass Spectrometry,
Sacoglossan sea slugs,
Galactolipids,
Sulfolipids
Conference:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) , Braga, Portugal, 9 Sep - 12 Sep, 2019.
Presentation Type:
Oral Presentation
Topic:
Ecology, Biodiversity and Vulnerable Ecosystems
Citation:
Rey
F,
Cartaxana
P,
Calado
R,
Domingues
M and
Cruz
S
(2019). Lipidomics of solar-power animals: a tool to unravel the process of kleptoplasty.
Front. Mar. Sci.
Conference Abstract:
XX Iberian Symposium on Marine Biology Studies (SIEBM XX) .
doi: 10.3389/conf.fmars.2019.08.00030
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Received:
29 Apr 2019;
Published Online:
27 Sep 2019.
*
Correspondence:
Dr. Felisa Rey, Department of Biology, University of Aveiro, Aveiro, 3810-193, Portugal, felisa.rey@gmail.com