Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
received:
17
06
2021
accepted:
22
09
2021
revised:
19
09
2021
pubmed:
13
10
2021
medline:
12
3
2022
entrez:
12
10
2021
Statut:
ppublish
Résumé
Foraminifera are ubiquitously distributed in marine habitats, playing a major role in marine sediment carbon sequestration and the nitrogen cycle. They exhibit a wide diversity of feeding and behavioural strategies (heterotrophy, autotrophy and mixotrophy), including species with the ability of sequestering intact functional chloroplasts from their microalgal food source (kleptoplastidy), resulting in a mixotrophic lifestyle. The mechanisms by which kleptoplasts are integrated and kept functional inside foraminiferal cytosol are poorly known. In our study, we investigated relationships between feeding strategies, kleptoplast spatial distribution and photosynthetic functionality in two shallow-water benthic foraminifera (Haynesina germanica and Elphidium williamsoni), both species feeding on benthic diatoms. We used a combination of observations of foraminiferal feeding behaviour, test morphology, cytological TEM-based observations and HPLC pigment analysis, with non-destructive, single-cell level imaging of kleptoplast spatial distribution and PSII quantum efficiency. The two species showed different feeding strategies, with H. germanica removing diatom content at the foraminifer's apertural region and E. williamsoni on the dorsal site. All E. williamsoni parameters showed that this species has higher autotrophic capacity albeit both feeding on benthic diatoms. This might represent two different stages in the evolutionary process of establishing a permanent symbiotic relationship, or may reflect different trophic strategies.
Identifiants
pubmed: 34635793
doi: 10.1038/s41396-021-01128-0
pii: 10.1038/s41396-021-01128-0
pmc: PMC8857221
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
822-832Informations de copyright
© 2021. The Author(s).
Références
Schiebel R. Planktic foraminiferal sedimentation and the marine calcite budget. Glob Biogeochem Cycl. 2002;16:1–21.
doi: 10.1029/2001GB001459
Lampitt RS, Salter I, John D. Radiolaria: major exporters of organic carbon to the deep ocean. Glob Biogeochem Cycl. 2009;23:GB1010.
doi: 10.1029/2008GB003221
Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MSM, Op den Camp HJM, et al. Evidence for complete denitrification in a benthic foraminifer. Nature. 2006;443:93–6.
pubmed: 16957731
doi: 10.1038/nature05070
Piña-Ochoa E, Hogslund S, Geslin E, Cedhagen T, Revsbech NP, Nielsen LP, et al. Widespread occurrence of nitrate storage and denitrification among foraminifera and gromiida. Proc Natl Acad Sci USA. 2010;107:1148–53.
pubmed: 20080540
doi: 10.1073/pnas.0908440107
Jauffrais T, LeKieffre C, Schweizer M, Geslin E, Metzger E, Bernhard JM, et al. Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub-cellular resolution. Environ Microbiol. 2019;21:125–41.
pubmed: 30277305
doi: 10.1111/1462-2920.14433
Delaca TE, Karl DM, Lipps JH. Direct use of dissolved organic-carbon by agglutinated benthic foraminifera. Nature. 1981;289:287–9.
doi: 10.1038/289287a0
Moodley L, Boschker HTS, Middelburg JJ, Pel R, Herman PMJ, de Deckere E, et al. Ecological significance of benthic foraminifera: C-13 labelling experiments. Mar Ecol Prog Ser. 2000;202:289–95.
doi: 10.3354/meps202289
LeKieffre C, Jauffrais T, Geslin E, Jesus B, Bernhard JM, Giovani ME, et al. Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer. Sci Rep. 2018;8:1–12.
doi: 10.1038/s41598-018-28455-1
Tsuchiya M, Chikaraishi Y, Nomaki H, Sasaki Y, Tame A, Uematsu K, et al. Compound-specific isotope analysis of benthic foraminifer amino acids suggests microhabitat variability in rocky-shore environments. Ecol Evol. 2018;8:8380–95.
pubmed: 30250710
pmcid: 6144965
doi: 10.1002/ece3.4358
Glock N, Roy AS, Romero D, Wein T, Weissenbach J, Revsbech NP, et al. Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA. 2019;116:2860–5.
pubmed: 30728294
pmcid: 6386669
doi: 10.1073/pnas.1813887116
Woehle C, Roy AS, Glock N, Wein T, Weissenbach J, Rosenstiel P, et al. A novel eukaryotic denitrification pathway in foraminifera. Curr Biol. 2018;28:1–8.
doi: 10.1016/j.cub.2018.06.027
Gooday A. Meiofaunal foraminiferans from the bathyal porcupine seabight (northeast Atlantic): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Res Part A Oceanogr Res Pap. 1986;33:1345–73.
doi: 10.1016/0198-0149(86)90040-3
Pascal P-Y, Dupuy C, Richard P, Mallet C, Telet EAC, Niquilb N. Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol Oceanogr. 2009;54:1048–59.
doi: 10.4319/lo.2009.54.4.1048
Jauffrais T, LeKieffre C, Schweizer M, Jesus B, Metzger E, Geslin E. Response of a kleptoplastidic foraminifer to heterotrophic starvation: photosynthesis and lipid droplet biogenesis. FEMS Microbiol Ecol. 2019;95:fiz046.
pubmed: 30947330
doi: 10.1093/femsec/fiz046
Grzymski J, Schofield OM, Falkowski PG, Bernhard JM. The function of plastids in the deep-sea benthic foraminifer, Nonionella stella. Limnol Oceanogr. 2002;47:1569–80.
doi: 10.4319/lo.2002.47.6.1569
Pillet L, de Vargas C, Pawlowski J. Molecular identification of sequestered diatom chloroplasts and kleptoplastidy in foraminifera. Protist. 2011;162:394–404.
pubmed: 21130034
doi: 10.1016/j.protis.2010.10.001
Cesbron F, Geslin E, Le Kieffre C, Jauffrais T, Nardelli MP, Langlet D, et al. Sequestered chloroplasts in the benthic foraminifer Haynesina germanica: cellular organization, oxygen fluxes and potential ecological implications. J Foraminifer Res. 2017;47:268–78.
doi: 10.2113/gsjfr.47.3.268
Jauffrais T, Jesus B, Metzger E, Mouget JL, Jorissen F, Geslin E. Effect of light on photosynthetic efficiency of sequestered chloroplasts in intertidal benthic foraminifera (Haynesina germanica and Ammonia tepida). Biogeosciences. 2016;13:2715–26.
doi: 10.5194/bg-13-2715-2016
Lopez E. Algal chloroplasts in the protoplasm of three species of benthic foraminifera: taxonomic affinity, viability and persistence. Mar Biol. 1979;53:201–11.
doi: 10.1007/BF00952427
Clark KB, Jensen KR, Stirts HM. Survey for functional kleptoplasty among West Atlantic Ascoglossa (=Sacoglossa) (Mollusca: Opisthobranchia). Veliger. 1990;33:339–45.
Rumpho ME, Dastoor F, Manhart J, Lee J. The kleptoplast. In: Wise RR, Hoober JK, editors. The structure and function of plastids. 23. New York: Advances in Photosynthesis and Respiration; 2006. p. 451–73.
doi: 10.1007/978-1-4020-4061-0_23
Jesus B, Ventura P, Calado G. Behaviour and a functional xanthophyll cycle enhance photo-regulation mechanisms in the solar-powered sea slug Elysia timida (Risso, 1818). J Exp Mar Biol Ecol. 2010;395:98–105.
doi: 10.1016/j.jembe.2010.08.021
Hansen PJ, Fenchel T. The bloom-forming ciliate Mesodinium rubrum harbours a single permanent endosymbiont. Mar Biol Res. 2006;2:169–77.
doi: 10.1080/17451000600719577
Hansen PJ, Ojamäe K, Berge T, Trampe EC, Nielsen LT, Lips I, et al. Photoregulation in a kleptochloroplastidic dinoflagellate Dinophysis acuta. Front Microbiol. 2016;7:1–11.
doi: 10.3389/fmicb.2016.00785
Decelle J, Colin S, Foster RA. Photosymbiosis in Marine Planktonic Protists. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F, editors. Marine Protists. Tokyo: Springer; 2015. p. 465–500.
doi: 10.1007/978-4-431-55130-0_19
Stoecker DK, Johnson MD, deVargas C, Not F. Acquired phototrophy in aquatic protists. Aquat Micro Ecol. 2009;57:279–310.
doi: 10.3354/ame01340
Rumpho ME, Summer EJ, Manhart JR. Solar-powered sea slugs. Mollusc/algal chloroplast symbiosis. Plant Physiol. 2000;123:29–38.
pubmed: 10806222
pmcid: 1539252
doi: 10.1104/pp.123.1.29
Park MG, Park JS, Kim M, Yih W. Plastids dynamics during survival of Dinophysis caudate without its ciliate prey. J Phycol. 2008;44:1154–63.
pubmed: 27041712
doi: 10.1111/j.1529-8817.2008.00579.x
Alexander SP, Banner FT. The functional relationship between skeleton and cytoplasm in Haynesina germanica (Ehrenberg). J Foraminifer Res. 1984;14:159–70.
doi: 10.2113/gsjfr.14.3.159
Bernhard JM, Alve E. Survival, ATP pool, and ultrastructural characterization of benthic foraminifera from Drammens fjord (Norway): Response to anoxia. Mar Micropaleontol. 1996;28:5–17.
doi: 10.1016/0377-8398(95)00036-4
Bernhard JM, Bowser SS. Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth Sci Rev. 1999;46:149–65.
doi: 10.1016/S0012-8252(99)00017-3
Bernhard JM, Buck KR, Farmer MA, Bowser SS. The Santa Barbara Basin is a symbiosis oasis. Nature. 2000;403:77–80.
pubmed: 10638755
doi: 10.1038/47476
Correia MJ, Lee JJ. Chloroplast retention by Elphidium excavatum (Terquem). Is it a selective process? Symbiosis. 2000;29:343–55.
Lee JJ, Lanners E, Ter Kuile B. The retention of chloroplasts by the foraminifera Elphidium crispum. Symbiosis. 1988;5:45–60.
Cedhagen T. Retention of chloroplasts and bathymetric distribution in the sublittoral foraminiferan Nonionellina labradorica. Ophelia. 1991;33:17–30.
doi: 10.1080/00785326.1991.10429739
Correia MJ, Lee JJ. Fine structure of the plastids retained by the foraminifer Elphidium excavatum (Terquem). Symbiosis. 2002;32:15–26.
Correia MJ, Lee JJ. How long do the plastids retained by Elphidium excavatum (Terquem) last in their host? Symbiosis. 2002;32:27–37.
Goldstein ST, Bernhard JM, Richardson EA. Chloroplast sequestration in the foraminifer Haynesina germanica: application of high pressure freezing and freeze substitution. Microsc Microanal. 2004;10:1458–9.
doi: 10.1017/S1431927604885891
Jauffrais T, LeKieffre C, Koho KA, Tsuchiya M, Schweizer M, Bernhard JM, et al. Ultrastructure and distribution of kleptoplasts in benthic foraminifera from shallow-water (photic) habitats. Mar Micropaleontol. 2018;138:46–62.
doi: 10.1016/j.marmicro.2017.10.003
Tsuchiya M, Toyofuku T, Uematsu K, Brüchert V, Collen J, Yamamoto H, et al. Cytologic and genetic characteristics of endobiotic bacteria and kleptoplasts of Virgulinella fragilis (Foraminifera). J Euk Microbiol. 2015;62:454–69.
pubmed: 25510528
doi: 10.1111/jeu.12200
Tsuchiya M, Miyawaki S, Oguri K, Toyofuku T, Tame A, Uematsu K, et al. Acquisition, Maintenance, and Ecological Roles of Kleptoplasts in Planoglabratella opercularis (Foraminifera, Rhizaria). Front Mar Sci. 2020;7:585.
doi: 10.3389/fmars.2020.00585
Jauffrais T, Jesus B, Méléder V, Geslin E. Functional xanthophyll cycle and pigment content of a kleptoplastic benthic foraminifer: Haynesina germanica. PLOS ONE. 2017;12:e0172678.
pubmed: 28231315
pmcid: 5322967
doi: 10.1371/journal.pone.0172678
Austin HA, Austin WE, Paterson DM. Extracellular cracking and content removal of the benthic diatom Pleurosigma angulatum (Quekett) by the benthic foraminifera Haynesina germanica (Ehrenberg). Mar Micropaleontol. 2005;57:68–73.
doi: 10.1016/j.marmicro.2005.07.002
Green BJ, Li WY, Manhart JR, Fox TC, Summer EJ, Kennedy RA, et al. Mollusc-algal chloroplast endosymbiosis. Photosynthesis, thylakoid protein maintenance, and chloroplast gene expression continue for many months in the absence of the algal nucleus. Plant Physiol. 2000;124:331–42.
pubmed: 10982447
pmcid: 59147
doi: 10.1104/pp.124.1.331
Nagai S, Nitshitani G, Tomaru Y, Sakiyama S, Kamiyama T. Predation by the toxic dinoflagellate Dinophysis fortii on the ciliate Myrionecta rubra and observation of sequestration of ciliate chloroplasts. J Phycol. 2008;44:909–22.
pubmed: 27041609
doi: 10.1111/j.1529-8817.2008.00544.x
Shi LX, Theg SM. The chloroplast protein import system: From algae to trees. Biochim Biophys Acta. 2013;1833:314–31.
pubmed: 23063942
doi: 10.1016/j.bbamcr.2012.10.002
de Vries J, Habicht J, Woehle C, Huang C, Christa G, Waegele H, et al. Is ftsH the key to plastid longevity in sacoglossan slugs? Genome Biol Evol. 2013;5:2540–8.
pubmed: 24336424
pmcid: 3879987
doi: 10.1093/gbe/evt205
Cruz S, Cartaxana P, Newcomer R, Dionísio G, Calado R, Serôdio J, et al. Photoprotection in sequestered plastids of sea slugs and respective algal sources. Sci Rep. 2015;5:1–8.
doi: 10.1038/srep07904
Cartaxana P, Morelli L, Jesus B, Calado G, Calado R, Cruz S. The photon menace: kleptoplast protection in the photosynthetic sea slug Elysia timida. J Exp Biol. 2019;222:jeb202580.
pubmed: 31171599
doi: 10.1242/jeb.202580
Petrou K, Ralph P, Nielsen D. A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera. ISME J. 2017;11:453–62.
pubmed: 27801906
doi: 10.1038/ismej.2016.128
Darling KF, Schweizer M, Knudsen KL, Evans KM, Bird C, Roberts A, et al. The genetic diversity, phylogeography and morphology of Elphidiidae (Foraminifera) in the Northeast Atlantic. Mar Micropaleontol. 2016;129:1–23.
doi: 10.1016/j.marmicro.2016.09.001
Kühl M, Polerecky L. Functional and structural imaging of aquatic phototrophic microbial communities and symbioses. Aquat Microb Ecol. 2008;53:99–118.
Rouse JW, Haas RH, Schell JA, Deering DW. Monitoring vegetation systems in the great plains with ERTS. Proc Third ERTS Symp. 1973;1:309–17.
Barillé L, Mouget JL, Méléder V, Rosa P, Jesus B. Spectral response of benthic diatoms with different sediment backgrounds. Remote Sens Environ. 2011;115:1034–42.
doi: 10.1016/j.rse.2010.12.008
Kazemipour F, Launeau P, Méléder V. Microphytobenthos biomass mapping using the optical model of diatom biofilms: application to hyperspectral images of Bourgneuf Bay. Remote Sens Environ. 2012;127:1–13.
doi: 10.1016/j.rse.2012.08.016
Meleder V, Barille L, Launeau P, Carrere V, Rince Y. Spectrometric constraint in analysis of benthic diatom biomass using monospecific cultures. Remote Sens Environ. 2003;88:386–400.
doi: 10.1016/j.rse.2003.08.009
Serôdio J, Pereira S, Furtado J, Silva R, Coelho H, Calado R. In vivo quantification of kleptoplastic chlorophyll a content in the “solar-powered” sea slug Elysia viridis using optical methods: spectral reflectance analysis and PAM fluorometry. Photochem Photobiol Sci. 2010;9:68–77.
pubmed: 20062846
doi: 10.1039/b9pp00058e
Jesus B, Mouget J-L, Perkins RG. Detection of diatom xanthophyll cycle using spectral reflectance. J Phycol. 2008;44:1349–59.
pubmed: 27041732
doi: 10.1111/j.1529-8817.2008.00583.x
Jesus B, Rosa P, Mouget JL, Méléder V, Launeau P, Barillé L. Spectral-radiometric analysis of taxonomically mixed microphytobenthic biofilms. Remote Sens Environ. 2014;140:196–205.
doi: 10.1016/j.rse.2013.08.040
Louchard EM, Reid RP, Stephens CF, Davis CO, Leathers RA, Downes TV, et al. Derivative analysis of absorption features in hyperspectral remote sensing data of carbonate sediments. Opt Express. 2002;10:1573–84.
pubmed: 19461694
doi: 10.1364/OE.10.001573
Perkins RG, Williamson CJ, Brodie J, Barillé L, Launeau P, Lavaud J, et al. Microspatial variability in community structure and photophysiology of calcified macroalgal microbiomes revealed by coupling of hyperspectral and high-resolution fluorescence imaging. Sci Rep. 2016;6:1–14.
doi: 10.1038/srep22343
Trampe E, Kolbowski J, Schreiber U, Kühl M. Rapid assessment of different oxygenic phototrophs and single-cell photosynthesis with multicolour variable chlorophyll fluorescence imaging. Mar Biol. 2011;158:1667–75.
doi: 10.1007/s00227-011-1663-1
Ralph PJ, Schreiber U, Gademann R, Kühl M, Larkum AWD. Coral photobiology studied with a new imaging pulse imaging pulse amplitude modulated fluorometer. J Phycol. 2005;41:335–42.
doi: 10.1111/j.1529-8817.2005.04034.x
Platt T, Gallegos CL, Harrison WG. Photoinhibition of photosynthesis in natural assemblages of marine phytoplancton. J Mar Res. 1980;38:687–701.
Kühl M, Glud RN, Borum J, Roberts R, Rysgaard S. Photosynthetic performance of surface associated algae below sea ice as measured with a pulse amplitude modulated (PAM) fluorometer and O2 microsensors. Mar Ecol Progr Ser S. 2001;223:1–14.
doi: 10.3354/meps223001
Harrison WG, Platt T. Photosynthesis-irradiance relationships in polar and temperate phytoplankton populations. Polar Biol. 1986;5:153–64.
doi: 10.1007/BF00441695
Elzhov TV, Mullen KM, Spiess A-N, Bolker B minpack.lm: R Interface to the Levenberg-Marquardt Nonlinear Least-Squares Algorithm Found in MINPACK, Plus Support for Bounds. 2016 R package version 1.2-1. https://CRAN.R-project.org/package=minpack.lm .
LeKieffre C, Spangenberg JE, Mabilleau G, Escrig S, Meibom A, Geslin E. Surviving anoxia in marine sediments: the metabolic response of ubiquitous benthic foraminifera (Ammonia tepida). PLOS ONE. 2017;12:e0177604.
pubmed: 28562648
pmcid: 5451005
doi: 10.1371/journal.pone.0177604
Bernhard JM. Distinguishing live from dead foraminifera: Methods review and proper applications. Micropaleontol. 2000;46:38–46.
Nomaki H, Bernhard JM, Ishida A, Tsuchiya M, Uematsu K, Tame A, et al. Intracellular isotope localization in Ammonia sp. (Foraminifera) of oxygen-depleted environments: results of nitrate and sulfate labeling experiments. Front Microbiol. 2016;7:1–12.
doi: 10.3389/fmicb.2016.00163
Eaton JW, Moss B. Estimation of numbers and pigment content in epipelic algal populations. Limnol Oceanogr. 1966;11:584–95.
doi: 10.4319/lo.1966.11.4.0584
Schneider CA, Rasband WS, Eliceiri K. NIH Image to ImageJ: 25 years of image analysis. Nat Meth. 2012;9:671–5.
doi: 10.1038/nmeth.2089
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing 2017, Vienna, Austria. URL https://www.R-project.org/ .
Schneider LK, Anestis K, Mansour J, Anschütz AA, Gypens N, Hansen PJ, et al. A dataset on trophic modes of aquatic protists. Biodivers Data J. 2020;8:e56648.
pubmed: 33177947
pmcid: 7599203
doi: 10.3897/BDJ.8.e56648
Banner FT, Culver SJ. Quaternary Haynesina n. gen. and paleogene Protelphidium Haynes; their morphology, affinities and distribution. J Foraminifer Res. 1978;8:177–207.
doi: 10.2113/gsjfr.8.3.177
Hansen HJ, Lykke-Andersen AL. Wall structure and classification of fossil and recent elphidiid and nonionid Foraminifera. Foss Strat. 1976;10:1–37.
Hottinger L, Reiss Z, Langer M. Spiral canals of some Elphidiidae. Micropaleontol. 2001;47:5–34.
Lee J. On a piece of chalk - Update. J Euk Microbiol. 1993;40:395–410.
doi: 10.1111/j.1550-7408.1993.tb04934.x
Passarelli C, Meziane T, Thiney N, Boeuf D, Jesus B, et al. Seasonal variations of the composition of microbial biofilms in sandy tidal flats: Focus of fatty acids, pigments and exopolymers. Estuar Coast Shelf Sci. 2015;153:29–37.
doi: 10.1016/j.ecss.2014.11.013
Jauffrais T, Drouet S, Turpin V, Méléder V, Jesus B, Cognie B, et al. Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings. J Exp Mar Biol Ecol. 2015;469:83–92.
doi: 10.1016/j.jembe.2015.04.014
Jauffrais T, Jesus B, Méléder V, Turpin V, Russo ADAPG, Raimbault P, et al. Physiological and photophysiological responses of the benthic diatom Entomoneis paludosa (Bacillariophyceae) to dissolved inorganic and organic nitrogen in culture. Mar Biol. 2016;163:1–14.
doi: 10.1007/s00227-016-2888-9
Meleder V, Laviale M, Jesus B, Mouget JL, Lavaud J, Kazemipour F, et al. In vivo estimation of pigment composition and optical absorption cross-section by spectroradiometry in four aquatic photosynthetic micro-organisms. J Photochem Photobio B-Biol. 2013;129:115–24.
doi: 10.1016/j.jphotobiol.2013.10.005
Knight R, Mantoura RFC. Chlorophyll and carotenoid pigments in foraminifera and their symbiotic algae: analysis by high performance liquid chromatography. Mar Ecol Prog Ser. 1985;23:241–9.
doi: 10.3354/meps023241
Ralph PJ, Gademann R. Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot. 2005;82:222–37.
doi: 10.1016/j.aquabot.2005.02.006
Olaizola M, Yamamoto HY. Short term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J Phycol. 1994;30:606–12.
doi: 10.1111/j.0022-3646.1994.00606.x
Lavaud J, Rousseau B, Etienne A-L. General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol. 2004;40:130–7.
doi: 10.1046/j.1529-8817.2004.03026.x
Ventura P, Calado G, Jesus B. Photosynthetic efficiency and kleptoplast pigment diversity in the sea slug Thuridilla hopei (Vérany, 1853). J Exp Mar Biol Ecol. 2013;441:105–9.
doi: 10.1016/j.jembe.2013.01.022
Martin R, Walther P, Tomaschko KH. Variable retention of kleptoplast membranes in cells of sacoglossan sea slugs: plastids with extended, shortened and non-retained durations. Zoomorphology. 2015;134:523–9.
doi: 10.1007/s00435-015-0278-3
Bird C, Schweizer M, Roberts A, Austin WEN, Knudsen KL, Evans KM, et al. The genetic diversity, morphology, biogeography, and taxonomic designations of Ammonia (Foraminifera) in the Northeast Atlantic. Mar Micropaleontol. 2020;155:101726.
doi: 10.1016/j.marmicro.2019.02.001