Decoupling cell size homeostasis in diatoms from the geometrical constraints of the silica cell wall.
cell size regulation
cell wall
diatoms
homeostasis
silica
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
15 Apr 2024
15 Apr 2024
Historique:
received:
26
11
2023
accepted:
18
03
2024
medline:
16
4
2024
pubmed:
16
4
2024
entrez:
16
4
2024
Statut:
aheadofprint
Résumé
Unicellular organisms are known to exert tight control over their cell size. In the case of diatoms, abundant eukaryotic microalgae, two opposing notions are widely accepted. On the one hand, the rigid silica cell wall that forms inside the parental cell is thought to enforce geometrical reduction of the cell size. On the other hand, numerous exceptions cast doubt on the generality of this model. Here, we monitored clonal cultures of the diatom Stephanopyxis turris for up to 2 yr, recording the sizes of thousands of cells, in order to follow the distribution of cell sizes in the population. Our results show that S. turris cultures above a certain size threshold undergo a gradual size reduction, in accordance with the postulated geometrical driving force. However, once the cell size reaches a lower threshold, it fluctuates around a constant size using the inherent elasticity of cell wall elements. These results reconcile the disparate observations on cell size regulation in diatoms by showing two distinct behaviors, reduction and homeostasis. The geometrical size reduction is the dominant driving force for large cells, but smaller cells have the flexibility to re-adjust the size of their new cell walls.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : H2020 European Research Council
ID : 848339
Informations de copyright
© 2024 The Authors New Phytologist © 2024 New Phytologist Foundation.
Références
Annunziata R, Mele BH, Marotta P, Volpe M, Entrambasaguas L, Mager S, Stec K, d'Alcalà MR, Sanges R, Finazzi G et al. 2022. Trade‐off between sex and growth in diatoms: molecular mechanisms and demographic implications. Science Advances 8: 1–17.
Armbrust EV, Chisholm SW. 1992. Patterns of cell size change in a marine centric diatom; variability evolving from clonal isolates. Journal of Phycology 28: 146–156.
Assmy P, Hernández‐Becerril DU, Montresor M. 2008. Morphological variability and life cycle traits of the type species of the diatom genus Chaetoceros, C. dichaeta. Journal of Phycology 44: 152–163.
Bethge H. 1925. Melosira und ihre planktonbegleiter, 3rd edn. Jena, Germany: G. Fischer.
Chepurnov VA, Mann DG, Von Dassow P, Vanormelingen P, Gillard J, Inzé D, Sabbe K, Vyverman W. 2008. In search of new tractable diatoms for experimental biology. BioEssays 30: 692–702.
Chepurnov VA, Mann DG, Vyverman W, Sabbe K, Danielidis DB. 2002. Sexual reproduction, mating system, and protoplast dynamics of Seminavis (Bacillariophyceae). Journal of Phycology 38: 1004–1019.
Costello JC, Chisholm SW. 1981. The influence of cell size on the growth rate of Thalassiosira weissflogii. Journal of Plankton Research 3: 415–419.
D'Alelio D, Amato A, Luedeking A, Montresor M. 2009. Sexual and vegetative phases in the planktonic diatom Pseudo‐nitzschia multistriata. Harmful Algae 8: 225–232.
Desikachary TV, Rao VNR. 1973. Studies on Cyclotella meneghiniana Kütz – III. The frustule. Proceedings of the Indian Academy of Sciences – Section B 77: 78–91.
Drebes G. 1964. Uber den lebenszyklus der marinen Planktondiatomee Stephanopyxis turris (Centrales) und seine Steuerung im Experiment. Helgoländer Wissenschaftliche Meeresuntersuchungen 10: 153–154.
Egusa S. 1949. Size variations in planktonic diatoms and some considerations of their ecological significance. I. Skeletonema costatum and Biddulphia sinensis. Nippon Suisan Gakkaishi 15: 332–336.
Falciatore A, Mock T, eds. 2022. The molecular life of diatoms, 1st edn. Cham, Switzerland: Springer.
Findlay IWO. 1969. Cell size and spore formation in a clone of a centric diatom, Coscinodiscus pavillardii Forti. Phykos 8: 31–41.
French FW, Hargraves PE. 1986. Population dynamics of the spore‐forming diatom Leptocylindrus danicus in Narragansett Bay, Rhode Island. Journal of Phycology 22: 411–420.
Fuhrmann‐Lieker T, Kubetschek N, Ziebarth J, Klassen R, Seiler W. 2021. Is the diatom sex clock a clock? Journal of the Royal Society Interface 18: 20210146.
Geitler L. 1932. Der Formwechsel der pennaten Diatomeen (Kieselalgen). Archiv für Protistenkunde 78: 1–226.
Gross F. 1937. The life history of some marine plankton diatoms. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 228: 1–47.
de Haan D, Aram L, Peled‐Zehavi H, Addadi Y, Ben‐Joseph O, Rotkopf R, Elad N, Rechav K, Gal A. 2023. Exocytosis of the silicified cell wall of diatoms involves extensive membrane disintegration. Nature Communications 14: 480.
Hense I, Beckmann A. 2015. A theoretical investigation of the diatom cell size reduction‐restitution cycle. Ecological Modelling 317: 66–82.
Hildebrand M, Lerch SJL, Shrestha RP. 2018. Understanding diatom cell wall silicification – moving forward. Frontiers in Marine Science 5: 1–19.
Hillebrand H, Acevedo‐Trejos E, Moorthi SD, Ryabov A, Striebel M, Thomas PK, Schneider ML. 2022. Cell size as driver and sentinel of phytoplankton community structure and functioning. Functional Ecology 36: 276–293.
Jewson D, Kuwata A, Cros L, Fortuño JM, Estrada M. 2016. Morphological adaptations to small size in the marine diatom Minidiscus comicus. Scientia Marina 80: 89–96.
Jewson DH. 1992a. Life cycle of a Stephanodiscus sp. (Bacillariophyta). Journal of Phycology 28: 856–866.
Jewson DH. 1992b. Size reduction, reproductive strategy and the life cycle of a centric diatom. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 336: 191–213.
Jewson DH, Granin NG. 2015. Cyclical size change and population dynamics of a planktonic diatom, Aulacoseira baicalensis, in Lake Baikal. European Journal of Phycology 50: 1–19.
Jun S, Levin PA, Taheri‐Araghi S, Bradde S, Hill NS, Vergassola M, Paulsson J, Sauls JT. 2017. Cell‐size control and homeostasis in bacteria. Current Biology 27: 1392.
Kaczmarska I, Ehrman JM, Mills KE, Sutcliffe SG, Samanta B. 2022. Vegetative cell enlargement in selected centric diatom species – an alternative way to propagate an individual genotype. European Journal of Phycology 58: 315–332.
Kalfon‐Cohen E, Goldbart O, Schreiber R, Cohen SR, Barlam D, Lorenz T, Enyashin A, Seifert G. 2011. Radial compression studies of WS2 nanotubes in the elastic regime. Journal of Vacuum Science & Technology B 29: 021009.
Klapper F, Audoor S, Vyverman W, Pohnert G. 2021. Pheromone mediated sexual reproduction of pennate diatom Cylindrotheca closterium. Journal of Chemical Ecology 47: 504–512.
Koester JA, Brawley SH, Karp‐Boss L, Mann DG. 2007. Sexual reproduction in the marine centric diatom Ditylum brightwellii (Bacillariophyta). European Journal of Phycology 42: 351–366.
Kroger N, Poulsen N. 2008. Diatoms – from cell wall biogenesis to nanotechnology. Annual Review of Genetics 42: 83–107.
Lewis WM. 1984. The diatom sex clock and its evolutionary significance. American Naturalist 123: 73–80.
Litchman E, Klausmeier CA, Yoshiyama K. 2009. Contrasting size evolution in marine and freshwater diatoms. Proceedings of the National Academy of Sciences, USA 106: 2665–2670.
Lucas CE, Stubbings HG. 1948. Continuous plankton records: size variations in diatoms and their ecological significance. Hull Bulletins of Marine Ecology 2: 133–171.
MacDonald JD. 1869. I. – On the structure of the Diatomaceous frustule, and its genetic cycle. Annals and Magazine of Natural History 3: 1–8.
Mann DG. 1988. Why didn't Lund see sex in Asterionella? A discussion of the diatom life cycle in nature. Algae and the Aquatic Environment 29: 385–412.
Marañón E. 2015. Cell size as a key determinant of phytoplankton metabolism and community structure. Annual Review of Marine Science 7: 241–264.
Margalef R. 1969. Size of centric diatoms as an ecological indicator. Internationale Vereinigung für Theoretische und Angewandte Limnologie 17: 202–210.
Mayzel B, Aram L, Varsano N, Wolf SG, Gal A. 2021. Structural evidence for extracellular silica formation by diatoms. Nature Communications 12: 1–8.
Moeys S, Frenkel J, Lembke C, Gillard JT, Devos V, Van den Berge K, Bouillon B, Huysman MJ, De Decker S, Scharf J et al. 2016. A sex‐inducing pheromone triggers cell cycle arrest and mate attraction in the diatom Seminavis robusta. Scientific Reports 6: 1–13.
Nečas D, Klapetek P. 2012. Gwyddion: an open‐source software for SPM data analysis. Central European Journal of Physics 10: 181–188.
Nipkow F. 1927. Uber das Verhalten der Skelette planktischer Kieselalgen im geschichteten Tiefenschlamm das Zfirich‐und Baldeggersees. Zeitschrift fur Hydrologie, Hydrographie, Hydrobiologie 4: 71–120.
Nishikawa T, Hori Y, Tanida K, Imai I. 2007. Population dynamics of the harmful diatom Eucampia zodiacus Ehrenberg causing bleachings of Porphyra thalli in aquaculture in Harima‐Nada, the Seto Inland Sea, Japan. Harmful Algae 6: 763–773.
Nishikawa T, Yutaka H, Harada K, Imai I. 2013. Annual regularity of reduction and restoration of cell size in the harmful diatom Eucampia zodiacus, and its application to the occurrence prediction of nori bleaching. Plankton & Benthos Research 8: 166–170.
O'Farrell I, Tell G, Podlejski A. 2001. Morphological variability of Aulacoseira granulata (Ehr.) Simonsen (Bacillariophyceae) in the Lower Paraná River (Argentina). Limnology 2: 65–71.
Otsu N. 1979. A threshold selection method from gray‐level histograms. IEEE Transactions on Systems, Man, and Cybernetics: Systems 9: 62–66.
de Pablo PJ, Schaap IAT, MacKintosh FC, Schmidt CF. 2003. Deformation and collapse of microtubules on the nanometer scale. Physical Review Letters 91: 1–4.
Perez‐Martinez C, Cruz‐Pizarro L, Sanchez‐Castillo P. 1992. Auxosporulation in Cyclotella ocellata (Bacillariophyceae) under natural and experimental conditions. Journal of Phycology 28: 608–615.
Peter KH, Sommer U. 2013. Phytoplankton cell size reduction in response to warming mediated by nutrient limitation. PLoS ONE 8: 1–6.
Pfitzer E. 1869. Über den Bau und die Zellteilung der Diatomeen. Botanische Zeitung 27: 774–776.
Pfitzer E. 1871. Untersuchungen uber Bau und Entwicklung der Bacillariaceen (Diatomaceen). Bonn, Germany: A. Marcus.
R Core Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rao VNR. 1978. Studies on Cyclotella meneghiniana Kiitz. IV. Progressive diminution in cell size. Proceedings of the Indian Academy of Sciences – Section B 87: 1–15.
Reimann BEF. 1964. Deposition of silica inside a diatom cell. Experimental Cell Research 34: 605–608.
Reimann BEF, Leivin JC, Volcani BE. 1966. Studies on the biochemistry and fine structure of silica shell formation in diatoms. II. The structure of the cell wall of Navicula pelliculosa (Bréb.) Hilse. Journal of Phycology 2: 74–78.
Rose DT, Cox EJ. 2013. Some diatom species do not show a gradual decrease in cell size as they reproduce. Fundamental and Applied Limnology 182: 117–122.
Round FE. 1972. The problem of reduction of cell size during diatom cell division. Nova Hedwigia 23: 291–303.
Round FE. 1982. Auxospore structure, initial valves and the development of populations of Stephanodiscus in farmoor reservoir. Annals of Botany 49: 447–459.
Round FE, Crawford RM, Mann DG. 1990. Diatoms: biology and morphology of the genera. Cambridge, UK: Cambridge University Press.
RStudio Team. 2020. Rstudio: integrated development for R. Boston, MA, USA: PBC.
Schmoller KM. 2017. The phenomenology of cell size control. Current Opinion in Cell Biology 49: 53–58.
von Stosch HA. 1965. Manipulierung der Zellgröße von Diatomeen im experiment. Phycologia 5: 21–44.
von Stosch HA, Drebes G. 1964. Entwicklungsgeschichtliche Untersuchungen an zentrischen Diatomeen IV. Helgoland Marine Research 11: 209–257.
Von Dassow P, Chepurnov VA, Armbrust EV. 2006. Relationships between growth rate, cell size, and induction of spermatogenesis in the centric diatom Thalassiosira weissflogii (Bacillariophyta). Journal of Phycology 42: 887–899.
Wallich GC. 1860. On the development and structure of the diatom valve. Transactions of the Microscopical Society & Journal 8: 129–145.
Wang C, Baehr C, Lai Z, Gao Y, Lek S, Li X. 2015. Exploring temporal trend of morphological variability of a dominant diatom in response to environmental factors in a large subtropical river. Ecological Informatics 29: 96–106.
Wickham H. 2016. ggplot2: elegant graphics for data analysis. New York, NY, USA: Springer‐Verlag.
Wiedling S. 1948. Beiträge zur Kenntnis der vegetativen Vermehrung der Diatomeen. Botaniska Notiser 1948: 322–354.
Wimpenny BRS. 1956. The size of diatoms III. The cell width of Biddulphia sinensis Greville from the southern North Sea. Journal of the Marine Biological Association of the United Kingdom 35: 375–386.
Wimpenny RS. 1936. The size of diatoms. I. The diameter variation of Rhizosolenia styliformis Brightw. and R. alata Brightw. in particular and of pelagic marine diatoms in general. Journal of the Marine Biological Association of the United Kingdom 21: 29–60.
Wimpenny RS. 1946. The size of diatoms II. Further observations on Rhizosolenia styliformis (Brightwell). Journal of the Marine Biological Association of the United Kingdom 26: 271–284.
Wood MA, Everroad RC, Wingard LM. 2005. Measuring growth rates in microalgal cultures. In: Andersen RA, ed. Algal culturing techniques. Burlington, MA, USA: Elsevier, 269–285.
Xu S, Chen M, Feng T, Zhan L, Zhou L, Yu G. 2021. Use ggbreak to effectively utilize plotting space to deal with large datasets and outliers. Frontiers in Genetics 12: 1–7.