Algal Remodeling in a Ubiquitous Planktonic Photosymbiosis

Decelle, Johan; Stryhanyuk, Hryhoriy; Gallet, Benoît; Veronesi, Giulia; Schmidt, Matthias; Balzano, Sergio; Marro, Sophie; Uwizeye, Clarisse; Jouneau, Pierre‐Henri; Lupette, Josselin; Jouhet, Juliette; Maréchal, Éric; Schwab, Yannick; Schieber, Nicole L.; Tucoulou, R.; Richnow, Hans H.; Finazzi, Guido; Musat, Niculina

doi:10.1016/j.cub.2019.01.073

Cited by 53 publications

(82 citation statements)

References 81 publications

(92 reference statements)

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“…Sample preparation for electron microscopy. Sample preparation protocols were adapted from (Decelle et al, 2019) to optimize the contrast for 3D electron microscopy imaging and therefore facilitate image segmentation through pixel classification. Live cells were cryofixed using high-pressure freezing (HPM100, Leica) in which cells were subjected to a pressure of 210 MPa at -196°C, followed by freeze-substitution (EM ASF2, Leica).…”

Section: Methodsmentioning

confidence: 99%

“…However, optical microscopy studies have insufficient resolution to reveal microstructural features, emphasising the need to develop complementary imaging approaches to study the cellular and subcellular bases of phytoplankton physiology and cell biology. Recently, a few studies (Decelle et al, 2019;Engel et al, 2015;Flori et al, 2017) have highlighted the potential of 3D electron microscopy (EM) imaging to explore these fundamental aspects of phytoplankton. This is a critical aspect, since previous work has suggested, for instance, that the physiology and metabolism of diatoms are determined by their peculiar cell organisations and more particularly by the morphology and arrangement of key energy-producing machineries, such as the plastids and mitochondria (Bailleul et al, 2015;Flori et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Here, we present a complete imaging workflow to access the cellular and subcellular features of phytoplankton at the nanometric scale based on Focused Ion Beam -Scanning Electron Microscopy (FIB-SEM) (Hawes and Hummel, 2015;Narayan and Subramaniam, 2015;Titze and Genoud, 2016). This technique has already been applied successfully to provide 3D models of eukaryotic cells (Decelle et al, 2019;Flori et al, 2017;Gavelis et al, 2019). Although the spatial resolution of FIB-SEM (4-8 nm) is lower than the resolution of transmission electron microscopy (Engel et al, 2015;Wietrzynski et al, 2020), it has the advantage of providing contextual 3D images of whole cells at a specific time.…”

Section: Introductionmentioning

confidence: 99%

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In-cell quantitative structural imaging of phytoplankton using 3D electron microscopy

Uwizeye

Decelle

Jouneau

et al. 2020

Preprint

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Phytoplankton is a minor fraction of the global biomass playing a major role in primary production and climate. Despite improved understanding of phytoplankton diversity and genomics, we lack nanoscale subcellular imaging approaches to understand their physiology and cell biology. Here, we present a complete Focused Ion Beam -Scanning Electron Microscopy (FIB-SEM) workflow (from sample preparation to image processing) to generate nanometric 3D phytoplankton models. Tomograms of entire cells, representatives of six ecologically-successful phytoplankton unicellular eukaryotes, were used for quantitative morphometric analysis. Besides lineage-specific cellular architectures, we observed common features related to cellular energy management: i) conserved cell-volume fractions occupied by the different organelles; ii) consistent plastid-mitochondria interactions, iii) constant volumetric ratios in these energy-producing organelles. We revealed detailed subcellular features related to chromatin organization and to biomineralization. Overall, this approach opens new perspectives to study phytoplankton acclimation responses to abiotic and biotic factors at a relevant biological scale.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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In-cell quantitative structural imaging of phytoplankton using 3D electron microscopy

Uwizeye

Decelle

Jouneau

et al. 2020

Preprint

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“…The combination of stable isotope labelling and chemical imaging (mass spectrometry imaging such as secondary ion mass spectrometry and matrix-assisted laser desorption ionization, and synchrotron X-ray fluorescence) is particularly valuable in this context, as it enables the investigation of metabolic exchange between the different components of a holobiont (Musat et al 2016;Raina et al 2017). Finally, three-dimensional electron microscopy may help evaluate to what extent different components of a holobiont are physically integrated (Colin et al 2017;Decelle et al 2019), where high integration is one indication of highly specific interactions. All of these techniques can be employed in both marine and terrestrial systems, but in marine systems the high phylogenetic diversity of organisms adds to the complexity of adapting and optimizing these techniques.…”

Section: Emerging Methodologies To Approach the Complexity Of Holobiomentioning

confidence: 99%

A community perspective on the concept of marine holobionts: current status, challenges, and future directions

Dittami

Arboleda

Auguet

et al. 2019

Preprint

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Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a stable relationship, form the holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial sciences where appropriate. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g. the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. The most significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This will be crucial to decipher the roles of marine holobionts in biogeochemical cycles, but also developing concrete applications of the holobiont concept e.g. to increase yield or disease resistance in aquacultures or to protect and restore marine ecosystems through management projects.

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“…More particularly, chemical imaging can provide information about the homeostasis of the nutrients (e.g. ionome) at the subcellular level, therefore highlighting the metabolic capacity and needs of the host and the symbiont [2]. The ionome can also provide information about the quality of the energy that is transferred up the food web and exported to the deep ocean.…”

mentioning

confidence: 99%