Ignited competition: Impact of bioactive extracellular compounds on organelle functions and photosynthetic systems in harmful algal blooms.
FPA‐FTIR
algal physiology
bioactive extracellular compounds
harmful algae
interspecies interaction
pyrenoid
thylakoid
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
24 Jul 2024
24 Jul 2024
Historique:
revised:
14
06
2024
received:
07
03
2024
accepted:
15
07
2024
medline:
26
7
2024
pubmed:
26
7
2024
entrez:
24
7
2024
Statut:
aheadofprint
Résumé
Prevalent interactions among marine phytoplankton triggered by long-range climatic stressors are well-known environmental disturbers of community structure. Dynamic response of phytoplankton physiology is likely to come from interspecies interactions rather than direct climatic effect on single species. However, studies on enigmatic interactions among interspecies, which are induced by bioactive extracellular compounds (BECs), especially between related harmful algae sharing similar shellfish toxins, are scarce. Here, we investigated how BECs provoke the interactions between two notorious algae, Alexandrium minutum and Gymnodinium catenatum, which have similar paralytic shellfish toxin (PST) profiles. Using techniques including electron microscopy and transcriptome analysis, marked disruptions in G. catenatum intracellular microenvironment were observed under BECs pressure, encompassing thylakoid membrane deformations, pyrenoid matrix shrinkage and starch sheaths disappearance. In addition, the upregulation of gene clusters responsible for photosystem-I Lhca1/4 and Rubisco were determined, leading to weaken photon captures and CO
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Key Research and Development Program of China
ID : 2019YFE0124700
Organisme : Scientific Research Foundation of Third Institute of Oceanography, Ministry of Natural Resources
ID : 2019002
Organisme : Bundesministerium für Bildung und Forschung
ID : 01LP2007A
Informations de copyright
© 2024 John Wiley & Sons Ltd.
Références
Allain, A.F., Paquin, P. & Subirade, M. (1999) Relationships between conformation of β‐lactoglobulin in solution and gel states as revealed by attenuated total reflection Fourier transform infrared spectroscopy. International Journal of Biological Macromolecules, 26(5), 337–344.
Baker, M.J., Trevisan, J., Bassan, P., Bhargava, R., Butler, H.J., Dorling, K.M. et al. (2014) Using Fourier transform IR spectroscopy to analyze biological materials. Nature Protocols, 9(8), 1771–1791.
Band‐Schmidt, C.J. (2004) Effects of growth medium, temperature, salinity and seawater source on the growth of Gymnodinium catenatum (Dinophyceae) from Bahia Concepcion, Gulf of California, Mexico. Journal of Plankton Research, 26(12), 1459–1470.
Band‐Schmidt, C.J., Bustillos‐Guzmán, J., Gárate‐Lizárraga, I., Lechuga‐Devéze, C.H., Reinhardt, K. & Luckas, B. (2005) Paralytic shellfish toxin profile in strains of the dinoflagellate Gymnodinium catenatum Graham and the scallop Argopecten ventricosus G.B. sowerby II from Bahı́a Concepción, Gulf of California, Mexico. Harmful algae, 4(1), 21–31.
Barber, J. & Gounaris, K. (1986) What role does sulpholipid play within the thylakoid membrane? Photosynthesis Research, 9(1–2), 239–249.
Bravo, I., Fraga, S., Isabel Figueroa, R., Pazos, Y., Massanet, A. & Ramilo, I. (2010) Bloom dynamics and life cycle strategies of two toxic dinoflagellates in a coastal upwelling system (NW Iberian Peninsula). Deep Sea Research Part II: Topical Studies in Oceanography, 57(3–4), 222–234.
Britton, D., Schmid, M., Noisette, F., Havenhand, J.N., Paine, E.R., McGraw, C.M. et al. (2020) Adjustments in fatty acid composition is a mechanism that can explain resilience to marine heatwaves and future ocean conditions in the habitat‐forming seaweed Phyllospora comosa(Labillardière) C.Agardh. Global Change Biology, 26(6), 3512–3524.
Burson, A., Stomp, M., Greenwell, E., Grosse, J. & Huisman, J. (2018) Competition for nutrients and light: testing advances in resource competition with a natural phytoplankton community. Ecology, 99(5), 1108–1118.
Cabrerizo, M.J., Álvarez‐Manzaneda, M.I., León‐Palmero, E., Guerrero‐Jiménez, G., de Senerpont Domis, L.N., Teurlincx, S. et al. (2020) Warming and CO2 effects under oligotrophication on temperate phytoplankton communities. Water Research, 173, 115579.
Chatchawal, P., Wongwattanakul, M., Tippayawat, P., Jearanaikoon, N., Jumniansong, A., Boonmars, T. et al. (2020) Monitoring the progression of liver fluke‐induced cholangiocarcinoma in a hamster model using synchrotron FTIR microspectroscopy and focal plane array infrared imaging. Analytical Chemistry, 92(23), 15361–15369.
Clède, S., Policar, C. & Sandt, C. (2014) Fourier transform infrared (FT‐IR) spectromicroscopy to identify cell organelles: correlation with fluorescence staining in MCF‐7 breast cancer cells. Applied Spectroscopy, 68(1), 113–117.
Collén, J., Guisle‐Marsollier, I., Léger, J.J. & Boyen, C. (2007) Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytologist, 176(1), 45–55.
Del Cortona, A., Leliaert, F., Bogaert, K.A., Turmel, M., Boedeker, C., Janouškovec, J. et al. (2017) The plastid genome in cladophorales Green algae is encoded by hairpin chromosomes. Current Biology, 27(24), 3771–3782.e6.
Croce, R. & van Amerongen, H. (2020) Light harvesting in oxygenic photosynthesis: structural biology meets spectroscopy. Science, 369(6506), 933–993.
Djanaguiraman, M., Narayanan, S., Erdayani, E. & Prasad, P.V.V. (2020) Effects of high temperature stress during anthesis and grain filling periods on photosynthesis, lipids and grain yield in wheat. BMC Plant Biology, 20(1), 268.
Encinas‐Yánez, M.F., Band‐Schmidt, C.J., Zenteno‐Savín, T., Leyva‐Valencia, I., Fernández Herrera, L.J. & Palacios‐Mechetnov, E. (2024) Deleterious effects of free fatty acids and hydrogen peroxide towards the dinoflagellate Gymnodinium catenatum. Frontiers in Protistology, 2, 1302560.
Falkowski, P. (2012) Ocean science: the power of plankton. Nature, 483(7387), S17–S20.
Field, C.B., Behrenfeld, M.J., Randerson, J.T. & Falkowski, P. (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281(5374), 237–240.
Fung, M.F.K., Senterman, M.K., Mikhael, N.Z., Lacelle, S. & Wong, P.T.T. (1996) Pressure‐tuning Fourier transform infrared spectroscopic study of carcinogenesis in human endometrium. Biospectroscopy, 2(3), 155–165.
Garip, S., Bozoglu, F. & Severcan, F. (2007) Differentiation of mesophilic and thermophilic bacteria with Fourier transform infrared spectroscopy. Applied Spectroscopy, 61(2), 186–192.
Garmendia, M., Borja, Á., Franco, J. & Revilla, M. (2013) Phytoplankton composition indicators for the assessment of eutrophication in marine waters: present state and challenges within the european directives. Marine Pollution Bulletin, 66(1–2), 7–16.
Garrido, S., Riobó, P., Rial, P. & Rodríguez, F. (2023) Short‐term interactions of Noctiluca scintillans with the toxic dinoflagellates Dinophysis acuminata and Alexandrium minutum: growth, toxins and allelopathic effects. Toxins, 15(6), 373.
Van Gennip, S.J., Popova, E.E., Yool, A., Pecl, G.T., Hobday, A.J. & Sorte, C.J.B. (2017) Going with the flow: the role of ocean circulation in global marine ecosystems under a changing climate. Global Change Biology, 23(7), 2602–2617.
Girometta, C., Dondi, D., Baiguera, R.M., Bracco, F., Branciforti, D.S., Buratti, S. et al. (2020) Characterization of mycelia from wood‐decay species by TGA and IR spectroscopy. Cellulose, 27(11), 6133–6148.
Gong, Y., Wang, X., Indran, I.R., Zhang, S.‐J., Lv, Z., Li, J. et al. (2014) Phytoplankton blooms: an overlooked marine source of natural endocrine disrupting chemicals. Ecotoxicology and Environmental Safety, 107, 126–132.
Gruber, N. (2011) Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 369(1943), 1980–1996.
Guillard, R.R.L. & Ryther, J.H. (1962) Studies of marine planktonic Diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) gran. Canadian Journal of Microbiology, 8, 229–239.
Hallegraeff, G., Anderson, D., Davidson, K., Gianella, F., Hansen, P. & Hegaret, H. (2023) et al. Fish‐Killing Marine Alagal Blooms: Causative Organisms, Ichthyotoxic Mechanisms, Impacts and Mitigation: Ocean Best Practices.
Hallegraeff, G.M., Anderson, D.M., Belin, C., Bottein, M.YD., Bresnan, E., Chinain, M. et al. (2021) Perceived global increase in algal blooms is attributable to intensified monitoring and emerging bloom impacts. Communications Earth & Environment, 2(1), 117.
Hernández‐García, C.I. & Martínez‐Jerónimo, F. (2023) Changes in the morphology and cell ultrastructure of a microalgal community exposed to a commercial glyphosate formulation and a toxigenic cyanobacterium. Frontiers in Microbiology, 14, 1195776.
Hernández‐Sandoval, F.E., Bustillos‐Guzmán, J.J., Band‐Schmidt, C.J., Núñez‐Vázquez, E.J., López‐Cortés, D.J., Fernández‐Herrera, L.J. et al. (2022) Effect of different N:P ratios on the growth, toxicity, and toxin profile of Gymnodinium catenatum (Dinophyceae) strains from the Gulf of California. Toxins, 14(7), 501.
Higashi, Y., Okazaki, Y., Myouga, F., Shinozaki, K. & Saito, K. (2015) Landscape of the lipidome and transcriptome under heat stress in Arabidopsis thaliana. Scientific Reports, 5, 10533.
Hu, H., Zhang, J. & Chen, W. (2011) Competition of bloom‐forming marine phytoplankton at low nutrient concentrations. Journal of Environmental Sciences, 23(4), 656–663.
Iswarya, V., Bhuvaneshwari, M., Alex, S.A., Iyer, S., Chaudhuri, G., Chandrasekaran, P.T. et al. (2015) Combined toxicity of two crystalline phases (anatase and rutile) of titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquatic Toxicology, 161, 154–169.
Iwai, M., Takahashi, Y. & Minagawa, J. (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. The Plant Cell, 20(8), 2177–2189.
Joliot, P. & Joliot, A. (2006) Cyclic electron flow in C3 plants. Biochimica et Biophysica Acta (BBA) ‐ Bioenergetics, 1757(5–6), 362–368.
Kunyaboon, S., Thumanu, K., Park, J.W., Khongla, C. & Yongsawatdigul, J. (2021) Evaluation of lipid oxidation, volatile compounds and vibrational spectroscopy of silver carp (Hypophthalmichthys molitrix) during ice storage as related to the quality of its washed mince. Foods, 10(3), 495.
Lelong, A., Haberkorn, H., Le Goïc, N., Hégaret, H. & Soudant, P. (2011) A new insight into allelopathic effects of Alexandrium minutum on photosynthesis and respiration of the diatom Chaetoceros neogracile revealed by photosynthetic‐performance analysis and flow cytometry. Microbial Ecology, 62(4), 919–930.
Lewis, A.M., Coates, L.N., Turner, A.D., Percy, L. & Lewis, J. (2018) A review of the global distribution of Alexandrium minutum (Dinophyceae) and comments on ecology and associated paralytic shellfish toxin profiles, with a focus on Northern Europe. Journal of Phycology, 54(5), 581–598.
Liu, M., Gu, H., Krock, B., Luo, Z. & Zhang, Y. (2020) Toxic dinoflagellate blooms of Gymnodinium catenatum and their cysts in Taiwan Strait and their relationship to global populations. Harmful algae, 97, 101868.
Liu, M., Krock, B., Yu, R., Leaw, C.P., Lim, P.T., Ding, G. et al. (2022) Co‐occurrence of Alexandrium minutum (Dinophyceae) ribotypes from the Chinese and Malaysian coastal waters and their toxin production. Harmful algae, 115, 102238.
Liu, X., Chen, L., Zhang, G., Zhang, J., Wu, Y. & Ju, H. (2021) Spatiotemporal dynamics of succession and growth limitation of phytoplankton for nutrients and light in a large shallow lake. Water Research, 194, 116910.
Long, M., Krock, B., Castrec, J. & Tillmann, U. (2021a) Unknown extracellular and bioactive metabolites of the genus Alexandrium: a review of overlooked toxins. Toxins, 13(12), 905.
Long, M., Peltekis, A., Gonzalez‐Fernandez, C., Hegaret, H. & Bailleul, B. (2021b) Allelochemicals of Alexandrium minutum: kinetics of membrane disruption and photosynthesis inhibition in a co‐occurring diatom. Harmful algae, 103, 101997.
Lunde, C., Jensen, P.E., Haldrup, A., Knoetzel, J. & Scheller, H.V. (2000) The PSI‐H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature, 408(6812), 613–615.
Ma, H., Krock, B., Tillmann, U., Bickmeyer, U., Graeve, M. & Cembella, A. (2011) Mode of action of membrane‐disruptive lytic compounds from the marine dinoflagellate Alexandrium tamarense. Toxicon, 58(3), 247–258.
Mao, X.‐T., Xu, R.‐X., Gao, Y., Li, H.‐Y., Liu, J.‐S. & Yang, W.‐D. (2021) Allelopathy of Alexandrium pacificum on Thalassiosira pseudonana in laboratory cultures. Ecotoxicology and Environmental Safety, 215, 112123.
Mardones, J.I., Müller, M.N. & Hallegraeff, G.M. (2017) Toxic dinoflagellate blooms of Alexandrium catenella in Chilean fjords: a resilient winner from climate change. ICES Journal of Marine Science, 74(4), 988–995.
Megha, K.B., Swathi, S., Joseph, X., Vandana, U. & Mohanan, P.V. (2022) Cytocompatibility of pluronics F‐127 on adenocarcinomic human alveolar basal epithelial cells (A549 cells). Environmental Science and Pollution Research, 29(47), 71124–71135.
Melin, A.M., Perromat, A. & Deleris, G. (2001) Fourier‐transform infrared spectroscopy: a pharmacotoxicologic tool for in vivo monitoring radical aggression. Canadian Journal of Physiology and Pharmacology, 79(2), 158–165.
Meng, Y., Yao, C., Xue, S. & Yang, H. (2014) Application of Fourier transform infrared (FT‐IR) spectroscopy in determination of microalgal compositions. Bioresource Technology, 151, 347–354.
Minagawa, J. & Takahashi, Y. (2004) Structure, function and assembly of photosystem II and its light‐harvesting proteins. Photosynthesis Research, 82(3), 241–263.
Morisaki, N., Sprecher, H., Milo, G.E. & Cornwell, D.G. (1982) Fatty acid specificity in the inhibition of cell proliferation and its relationship to lipid peroxidation and prostaglandin biosynthesis. Lipids, 17(12), 893–899.
Ockendon, N., Baker, D.J., Carr, J.A., White, E.C., Almond, R.E.A., Amano, T. et al. (2014) Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Global Change Biology, 20(7), 2221–2229.
Pronina, N.A., Rogova, N.B., Furnadzhieva, S. & Klyachko‐Gurvich, G.L. (1998) Effect of CO2 concentration on the fatty acid composition of lipids in Chlamydomonas reinhardtii cia‐3, a mutant deficient in CO2‐concentrating mechanism. Russian Journal of Plant Physiology, 45(4), 447–455.
Ralston, D.K. & Moore, S.K. (2020) Modeling harmful algal blooms in a changing climate. Harmful algae, 91, 101729.
Sepúlveda, J. & Cantarero, S.I. (2022) Phytoplankton response to a warming ocean. Science, 376(6600), 1378–1379.
Simsek Ozek, N., Tuna, S., Erson‐Bensan, A.E. & Severcan, F. (2010) Characterization of microRNA‐125b expression in MCF7 breast cancer cells by ATR‐FTIR spectroscopy. The Analyst, 135(12), 3094–3102.
Su, X., Ma, J., Pan, X., Zhao, X., Chang, W., Liu, Z. et al. (2019) Antenna arrangement and energy transfer pathways of a green algal photosystem‐I‐LHCI supercomplex. Nature Plants, 5(3), 273–281.
Subirade, M., Gueguen, J. & Pézolet, M. (1994) Conformational changes upon dissociation of a globular protein from pea: a Fourier transform infrared spectroscopy study. Biochimica et Biophysica Acta (BBA) ‐ Protein Structure and Molecular Enzymology, 1205(2), 239–247.
Sui, N. & Han, G. (2014) Salt‐induced photoinhibition of PS II is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiologiae Plantarum, 36(4), 983–992.
Thangaraj, S., Liu, H., Kim, I.‐N. & Sun, J. (2022) Acclimation traits determine the macromolecular basis of harmful dinoflagellate Alexandrium minutum in response to changing climate conditions. Harmful algae, 118, 102313.
Tillmann, U. & John, U. (2002) Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP‐toxin content. Marine Ecology Progress Series, 230, 47–58.
Toyokawa, C., Yamano, T. & Fukuzawa, H. (2020) Pyrenoid starch sheath is required for LCIB localization and the CO2‐concentrating mechanism in green algae. Plant Physiology, 182(4), 1883–1893.
Treves, H., Küken, A., Arrivault, S., Ishihara, H., Hoppe, I., Erban, A. et al. (2022) Carbon flux through photosynthesis and central carbon metabolism show distinct patterns between algae, C‐3 and C‐4 plants. Nature Plants, 8(1), 78–91.
Vigneault, B., Percot, A., Lafleur, M. & Campbell, P.G.C. (2000) Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Environmental Science & Technology, 34(18), 3907–3913.
Wang, H., Zhang, Y., Zeng, K., Qiang, J., Cao, Y., Li, Y. et al. (2021) Selective mitochondrial protein labeling enabled by biocompatible photocatalytic reactions inside live cells. Jacs Au, 1(7), 1066–1075.
Wang, L. & Jonikas, M.C. (2020) The pyrenoid. Current Biology, 30(10), R456–R458.
Wang, R., Wang, J., Xue, Q., Sha, X., Tan, L. & Guo, X. (2017) Allelopathic interactions between Skeletonema costatum and Alexandrium minutum. Chemistry and Ecology, 33(6), 485–498.
Wang, S., Zhang, N., Xu, H., Tan, L. & Wang, J. (2024) Allelochemicals of Alexandrium tamarense and its algicidal mechanism for Prorocentrum donghaiense and Heterosigma akashiwo. Chemosphere, 357, 141953.
Wood, B.R., Quinn, M.A., Tait, B., Ashdown, M., Hislop, T., Romeo, M. et al. (1998) FTIR microspectroscopic study of cell types and potential confounding variables in screening for cervical malignancies. Biospectroscopy, 4(2), 75–91.
Wrobel, T.P., Mukherjee, P. & Bhargava, R. (2017) Rapid visualization of macromolecular orientation by discrete frequency mid‐infrared spectroscopic imaging. The Analyst, 142(1), 75–79.
Yang, W.D., Xie, J., van Rijssel, M., Li, H.Y. & Liu, J.S. (2010) Allelopathic effects of Alexandrium spp. on Prorocentrum donghaiense. Harmful algae, 10(1), 116–120.
Yano, K., Ohoshima, S., Gotou, Y., Kumaido, K., Moriguchi, T. & Katayama, H. (2000) Direct measurement of human lung cancerous and noncancerous tissues by Fourier transform infrared microscopy: can an infrared microscope be used as a clinical tool? Analytical Biochemistry, 287(2), 218–225.
Zalutskaya, Z.M., Skryabina, U.S. & Ermilova, E.V. (2019) Generation of hydrogen peroxide and transcriptional regulation of antioxidant enzyme expression in Chlamydomonas reinhardtii under hypothermia. Russian Journal of Plant Physiology, 66(2), 223–230.
Zhang, F., Yao, X., Sun, S., Wang, L., Liu, W., Jiang, X. et al. (2020) Effects of mesotrione on oxidative stress, subcellular structure, and membrane integrity in Chlorella vulgaris. Chemosphere, 247, 125668.