Subcellular architecture and metabolic connection in the planktonic photosymbiosis between Collodaria (radiolarians) and their microalgae.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
revised:
27
08
2021
received:
13
05
2021
accepted:
05
09
2021
pubmed:
10
9
2021
medline:
18
3
2022
entrez:
9
9
2021
Statut:
ppublish
Résumé
Photosymbiosis is widespread and ecologically important in the oceanic plankton but remains poorly studied. Here, we used multimodal subcellular imaging to investigate the photosymbiosis between colonial Collodaria and their microalga dinoflagellate (Brandtodinium). We showed that this symbiosis is very dynamic whereby symbionts interact with different host cells via extracellular vesicles within the colony. 3D electron microscopy revealed that the photosynthetic apparatus of the microalgae was more voluminous in symbiosis compared to free-living while the mitochondria volume was similar. Stable isotope probing coupled with NanoSIMS showed that carbon and nitrogen were stored in the symbiotic microalga in starch granules and purine crystals respectively. Nitrogen was also allocated to the algal nucleolus. In the host, low
Identifiants
pubmed: 34499794
doi: 10.1111/1462-2920.15766
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6569-6586Informations de copyright
© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Anderson, O.R. (1976) Ultrastructure of a colonial radiolarian Collozoum inerme and a cytochemical determination of the role of its zooxanthellae. Tissue Cell 8: 195-208.
Bhaud, Y., Guillebault, D., Lennon, J.F., Defacque, H., Soyer-Gobillard, M.O., and Moreau, H. (2000) Morphology and behaviour of dinoflagellate chromosomes during the cell cycle and mitosis. J Cell Sci 113: 1231-1239.
Biard, T., Bigeard, E., Audic, S., Poulain, J., Gutierrez-Rodriguez, A., Pesant, S., et al. (2017) Biogeography and diversity of Collodaria (Radiolaria) in the global ocean. ISME J 11: 1331-1344.
Biard, T., Stemmann, L., Picheral, M., Mayot, N., Vandromme, P., Hauss, H., et al. (2016) In situ imaging reveals the biomass of giant protists in the global ocean. Nature 532: 504-507.
Blank, R.J. (1987) Cell architecture of the dinoflagellate Symbiodinium sp. inhabiting the Hawaiian stony coral Montipora verrucosa. Mar Biol 94: 143-155.
Boncompain, G., and Perez, F. (2013) The many routes of Golgi-dependent trafficking. Histochem Cell Biol 140: 251-260.
Breitbarth, E., Wohlers, J., Kläs, J., LaRoche, J., and Peeken, I. (2008) Nitrogen fixation and growth rates of Trichodesmium IMS-101 as a function of light intensity. Mar Ecol Prog Ser 359: 25-36.
Cabello, A.M., Cornejo-Castillo, F.M., Raho, N., Blasco, D., Vidal, M., Audic, S., et al. (2016) Global distribution and vertical patterns of a prymnesiophyte-cyanobacteria obligate symbiosis. ISME J 10: 693-706.
Caron, D.A. (2016) Ocean science: the rise of Rhizaria. Nature 532: 444-445.
Caron, D.A., Michaels, A.F., Swanberg, N.R., and Howse, F.A. (1995) Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J Plankton Res 17: 103-129. https://doi.org/10.1093/plankt/17.1.103
Clode, P.L., Saunders, M., Maker, G., Ludwig, M., and Atkins, C.A. (2009) Uric acid deposits in symbiotic marine algae. Plant Cell Environ 32: 170-177.
Cotte, M., Pouyet, E., Salomé, M., Rivard, C., De Nolf, W., Castillo-Michel, H., et al. (2017) The ID21 X-ray and infrared microscopy beamline at the ESRF: status and recent applications to artistic materials. J Anal At Spectrom 32: 477-493.
Davy, S.K., Allemand, D., and Weis, V.M. (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76: 229-261.
de Vargas, C., Audic, S., Henry, N., Decelle, J., Mahe, F., Logares, R., et al. (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348: 1261605.
Decelle, J., Colin, S., and Foster, R.A. (2015) Photosymbiosis in marine planktonic protists. In Marine Protists: Diversity and Dynamics, Ohtsuka, S., Suzaki, T., Horiguchi, T., Suzuki, N., and Not, F. (eds). Japan, Tokyo: Springer, pp. 1-637. 10.1007/978-4-431-55130-0_19
Decelle, J., Probert, I., Bittner, L., Desdevises, Y., Colin, S., de Vargas, C., et al. (2012) An original mode of symbiosis in open ocean plankton. Proc Natl Acad Sci U S A 109: 18000-18005.
Decelle, J., Stryhanyuk, H., Gallet, B., Veronesi, G., Schmidt, M., Balzano, S., et al. (2019) Algal remodeling in a ubiquitous planktonic photosymbiosis. Curr Biol 29: 968-978.e4.
Decelle, J., Veronesi, G., Gallet, B., Stryhanyuk, H., Benettoni, P., Schmidt, M., et al. (2020) Subcellular chemical imaging: new avenues in cell biology. Trends Cell Biol 30: 173-188. https://doi.org/10.1016/j.tcb.2019.12.007
Dennett, M.R., Caron, D.A., Michaels, A.F., Gallager, S.M., and Davis, C.S. (2002) Video plankton recorder reveals high abundances of colonial radiolaria in surface waters of the central north pacific. J Plankton Res 24: 797-805. https://doi.org/10.1093/plankt/24.8.797
Engel, B.D., Schaffer, M., Cuellar, L.K., Villa, E., Plitzko, J.M., and Baumeister, W. (2015) Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. Elife 4: e04889.
Faure, E., Not, F., Benoiston, A.S., Labadie, K., Bittner, L., and Ayata, S.D. (2019) Mixotrophic protists display contrasted biogeographies in the global ocean. ISME J 13: 1072-1083.
Gautier, A., Michel-Salamin, L., Tosi-Couture, E., McDowall, A.W., and Dubochet, J. (1986) Electron microscopy of the chromosomes of dinoflagellates in situ: confirmation of Bouligand's liquid crystal hypothesis. J Ultrastruct Res Mol Struct Res 97: 10-30.
Geider, R., and La Roche, J. (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37: 1-17.
Genty, B., Briantais, J.M., and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta - Gen Subj 990: 87-92. https://doi.org/10.1016/S0304-4165(89)80016-9
Giordano, M., Norici, A., and Hell, R. (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166: 371-382. doi: 10.1111/j.1469-8137.2005.01335.x.
Gornik, S.G., Hu, I., Lassadi, I., and Waller, R.F. (2019) The biochemistry and evolution of the dinoflagellate nucleus. Microorganisms 7: 245.
Guidi, L., Chaffron, S., Bittner, L., Eveillard, D., Larhlimi, A., Roux, S., et al. (2016) Plankton networks driving carbon export in the oligotrophic ocean. Nature 532: 465-470.
Gutierrez-Rodriguez, A., Pillet, L., Biard, T., Said-Ahmad, W., Amrani, A., Simó, R., and Not, F. (2017) Dimethylated sulfur compounds in symbiotic protists: a potentially significant source for marine DMS(P). Limnol Oceanogr 62: 1139-1154.
Hennies, J., Lleti, J.M.S., Schieber, N.L., Templin, R.M., Steyer, A.M., and Schwab, Y. (2020) AMST: alignment to median smoothed template for focused ion beam scanning electron microscopy image stacks. Sci Rep 10: 1-10.
Karl, D.M., Church, M.J., Dore, J.E., Letelier, R.M., and Mahaffey, C. (2012) Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc Natl Acad Sci U S A 109: 1842-1849.
Kashiv, Y., Austin, J.R., Lai, B., Rose, V., Vogt, S., and El-Muayed, M. (2016) Imaging trace element distributions in single organelles and subcellular features. Sci Rep 6: 21437.
Kikinis, R., Pieper, S.D., and Vosburgh, K.G. (2014) 3D slicer: a platform for subject-specific image analysis, visualization, and clinical support. In Intraoperative imaging and image-guided therapy. New York, NY: Springer New York, pp. 277-289.
Kopp, C., Domart-Coulon, I., Escrig, S., Humbel, B.M., Hignette, M., and Meibom, A. (2015) Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. MBio 6: 1-9.
Kopp, C., Pernice, M., Domart-Coulon, I., Djediat, C., Spangenberg, J.E., Alexander, D.T.L., et al. (2013) Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. MBio 4: 1-9.
Lekieffre, C., Jauffrais, T., Geslin, E., Jesus, B., Bernhard, J.M., Giovani, M.E., and Meibom, A. (2018) Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer. Sci Rep 8: 1-12.
LeKieffre, C., Spero, H.J., Fehrenbacher, J.S., Russell, A.D., Ren, H., Geslin, E., and Meibom, A. (2020) Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts. Proc Biol Sci 287: 20200620.
Liu, Z., Mesrop, L.Y., Hu, S.K., and Caron, D.A. (2019) Transcriptome of Thalassicolla nucleata holobiont reveals details of a radiolarian symbiotic relationship. Front Mar Sci 6: 1-11.
Loussert-Fonta, C., Toullec, G., Paraecattil, A.A., Jeangros, Q., Krueger, T., Escrig, S., and Meibom, A. (2020) Correlation of fluorescence microscopy, electron microscopy, and NanoSIMS stable isotope imaging on a single tissue section. Commun Biol 3: 362.
Lowe, D.G. (2004) Distinctive image features from scale-invariant keypoints. Int J Comput Vis 60: 91-110.
Maco, B., Cantoni, M., Holtmaat, A., Kreshuk, A., Hamprecht, F.A., and Knott, G.W. (2014) Semiautomated correlative 3D electron microscopy of in vivo-imaged axons and dendrites. Nat Protoc 9: 1354-1366.
Maruyama, S., and Weis, V.M. (2021) Limitations of using cultured algae to study cnidarian-algal symbioses and suggestions for future studies. J Phycol 57: 30-38.
Matthews, J.L., Oakley, C.A., Lutz, A., Hillyer, K.E., Grossman, A.R., Weis, V.M., and Davy, S.K. (2018) Partner switching and metabolic flux in a model cnidarian - symbiodinium symbiosis. Proc R Soc B 285(1892). https://doi.org/10.1098/rspb.2018.2336
Martínez-Criado G., Villanova J., Tucoulou R., Salomon D., Suuronen J.-P., Labouré S., et al. (2016) ID16B: a hard X-ray nanoprobe beamline at the ESRF for nano-analysis. J Synchrotron Radiat, 23(1): 344-352. https://doi.org/10.1107/s1600577515019839
Maxwell, K., and Johnson, G.N. (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51: 659-668.
Mellman, I., and Simons, K. (1992) The Golgi complex: In vitro veritas?. Cell, 68(5): 829-840. https://doi.org/10.1016/0092-8674(92)90027-a
Meyer, M.T., Whittaker, C., and Griffiths, H. (2017) The algal pyrenoid: key unanswered questions. J Exp Bot 68: 3739-3749.
Mojzeš, P., Gao, L., Ismagulova, T., Pilátová, J., Moudříková, Š., Gorelova, O., et al. (2020) Guanine, a high-capacity and rapid-turnover nitrogen reserve in microalgal cells. Proc Natl Acad Sci U S A 117: 32722-32730.
Moore, C.M., Mills, M.M., Arrigo, K.R., Berman-Frank, I., Bopp, L., Boyd, P.W., et al. (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6: 701-710.
Moore, K.L., Lombi, E., Zhao, F.J., and Grovenor, C.R.M. (2012) Elemental imaging at the nanoscale: NanoSIMS and complementary techniques for element localisation in plants. Anal Bioanal Chem 402: 3263-3273.
Morel, F.M.M., Milligan, A.J., and Saito, M.A. (2003) Marine bioinorganic chemistry: the role of trace metals in the oceanic cycles of major nutrients. In Henry Elderfield (ed.), Treatise on Geochemistry, Vol. 6. Elsevier, pp. 113-143. https://doi.org/10.1016/B0-08-043751-6/06108-9
Morel, F.M.M., and Price, N.M. (2003) The biogeochemical cycles of trace metals in the oceans. Science 300: 944-947.
Passarelli, M.K., Pirkl, A., Moellers, R., Grinfeld, D., Kollmer, F., Havelund, R., et al. (2017) The 3D OrbiSIMS - label-free metabolic imaging with subcellular lateral resolution and high mass-resolving power. Nat Methods 14: 1175-1183.
Polerecky, L., Adam, B., Milucka, J., Musat, N., Vagner, T., and Kuypers, M.M.M. (2012) Look@NanoSIMS - a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol 14: 1009-1023.
Probert, I., Siano, R., Poirier, C., Decelle, J., Biard, T., Tuji, A., et al. (2014) Brandtodinium gen. nov. and B. nutricula comb. Nov. (Dinophyceae), a dinoflagellate commonly found in symbiosis with polycystine radiolarians. J Phycol 50: 388-399.
Rädecker, N., Pogoreutz, C., Voolstra, C.R., Wiedenmann, J., and Wild, C. (2015) Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol 23: 1-8.
Raina, J.B., Clode, P.L., Cheong, S., Bougoure, J., Kilburn, M.R., Reeder, A., et al. (2017) Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. Elife 6: 1-17.
Raina, J.B., Dinsdale, E.A., Willis, B.L., and Bourne, D.G. (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18: 101-108.
Reich, H.G. (2020) Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae Endosymbiotic dinoflagellates pump iron: differences in iron and other trace metal needs among the Symbiodiniaceae. Coral Reefs 39: 915-927.
Rodriguez, I.B., Lin, S., Ho, J., and Ho, T.Y. (2016) Effects of trace metal concentrations on the growth of the coral endosymbiont Symbiodinium kawagutii. Front Microbiol 7: 1-10.
Sbalzarini, I.F., and Koumoutsakos, P. (2005) Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182-195.
Simó, R. (2001) Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol 16: 287-294.
Solé, V.A., Papillon, E., Cotte, M., Walter, P., and Susini, J. (2007) A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim Acta - Part B At Spectrosc 62: 63-68.
Stryhanyuk, H., Calabrese, F., Kümmel, S., Musat, F., Richnow, H.H., and Musat, N. (2018) Calculation of single cell assimilation rates from sip-nanosims-derived isotope ratios: a comprehensive approach. Front Microbiol 9: 1-15.
Swanberg, N.R., and Caron, D.A. (1991) Patterns of sarcodine feeding in epipelagic oceanic plankton. J Plankton Res 13: 287-312.
Thompson, A.W., Foster, R.A., Krupke, A., Carter, B.J., Musat, N., Vaulot, D., et al. (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337: 1546-1550.
Twining, B.S., and Baines, S.B. (2013) The trace metal composition of marine phytoplankton. Ann Rev Mar Sci 5: 191-215.
Uwizeye, C., Decelle, J., Jouneau, P., Flori, S., Gallet, B., Keck, J., et al. (2021a) Morphological bases of phytoplankton energy management and physiological responses unveiled by 3D subcellular imaging. Nat Commun 12: 1049.
Uwizeye, C., Mars Brisbin, M., Gallet, B., Chevalier, F., Charlotte, L., Schieber, N., et al. (2021b) Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae. Proc Natl Acad Sci U S A 118: e2025252118. 10.1073/pnas.2025252118
Villar, E., Dani, V., Bigeard, E., Linhart, T., Mendez-Sandin, M., Bachy, C., et al. (2018) Symbiont chloroplasts remain active during bleaching-like response induced by thermal stress in Collozoum pelagicum (Collodaria, Retaria). Front Mar Sci 5: 1-11.