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      Judging Diatoms by Their Cover: Variability in Local Elasticity of Lithodesmium undulatum Undergoing Cell Division

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      1 , * , 2 , 3
      PLoS ONE
      Public Library of Science

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          Abstract

          Unique features of diatoms are their intricate cell covers (frustules) made out of hydrated, amorphous silica. The frustule defines and maintains cell shape and protects cells against grazers and pathogens, yet it must allow for cell expansion during growth and division. Other siliceous structures have also evolved in some chain-forming species as means for holding neighboring cells together. Characterization and quantification of mechanical properties of these structures are crucial for the understanding of the relationship between form and function in diatoms, but thus far only a handful of studies have addressed this issue. We conducted micro-indentation experiments, using atomic force microscopy (AFM), to examine local variations in elastic (Young's) moduli of cells and linking structures in the marine, chain-forming diatom Lithodesmium undulatum. Using a fluorescent tracer that is incorporated into new cell wall components we tested the hypothesis that new siliceous structures differ in elastic modulus from their older counterparts. Results show that the local elastic modulus is a highly dynamic property. Elastic modulus of stained regions was significantly lower than that of unstained regions, suggesting that newly formed cell wall components are generally softer than the ones inherited from the parent cells. This study provides the first evidence of differentiation in local elastic properties in the course of the cell cycle. Hardening of newly formed regions may involve incorporation of additional, possibly organic, material but further studies are needed to elucidate the processes that regulate mechanical properties of the frustule during the cell cycle.

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          Most cited references14

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          Architecture and material properties of diatom shells provide effective mechanical protection.

          Diatoms are the major contributors to phytoplankton blooms in lakes and in the sea and hence are central in aquatic ecosystems and the global carbon cycle. All free-living diatoms differ from other phytoplankton groups in having silicified cell walls in the form of two 'shells' (the frustule) of manifold shape and intricate architecture whose function and role, if any, in contributing to the evolutionary success of diatoms is under debate. We explored the defence potential of the frustules as armour against predators by measuring their strength. Real and virtual loading tests (using calibrated glass microneedles and finite element analysis) were performed on centric and pennate diatom cells. Here we show that the frustules are remarkably strong by virtue of their architecture and the material properties of the diatom silica. We conclude that diatom frustules have evolved as mechanical protection for the cells because exceptional force is required to break them. The evolutionary arms race between diatoms and their specialized predators will have had considerable influence in structuring pelagic food webs and biogeochemical cycles.
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            Measuring elasticity of biological materials by atomic force microscopy.

            Atomic force microscopy (AFM) has proved its value not only for resolving the topographical structure of biological samples, but also for probing inherent properties of biological structures, like local interaction forces, mechanical properties or dynamics in a natural (physiological) environment. This minireview focuses on the acquisition of elasticity data of biomaterials by AFM. A possible theoretical model is presented, followed by a practical 'how to do it with AFM', and, finally, a brief overview of publications in this field is given.
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              Chitin in diatoms and its association with the cell wall.

              Chitin is a globally abundant polymer widely distributed throughout eukaryotes that has been well characterized in only a few lineages. Diatoms are members of the eukaryotic lineage of stramenopiles. Of the hundreds of diatom genera, two produce long fibers of chitin that extrude through their cell walls of silica. We identify and describe here genes encoding putative chitin synthases in a variety of additional diatom genera, indicating that the ability to produce chitin is more widespread and likely plays a more central role in diatom biology than previously considered. Diatom chitin synthases fall into four phylogenetic clades. Protein domain predictions and differential gene expression patterns provide evidence that chitin synthases have multiple functions within a diatom cell. Thalassiosira pseudonana possesses six genes encoding three types of chitin synthases. Transcript abundance of the gene encoding one of these chitin synthase types increases when cells resume division after short-term silicic acid starvation and during short-term limitation by silicic acid or iron, two nutrient conditions connected in the environment and known to affect the cell wall. During long-term silicic acid starvation transcript abundance of this gene and one additional chitin synthase gene increased at the same time a chitin-binding lectin localized to the girdle band region of the cell wall. Together, these results suggest that the ability to produce chitin is more widespread in diatoms than previously thought and that a subset of the chitin produced by diatoms is associated with the cell wall.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                22 October 2014
                : 9
                : 10
                : e109089
                Affiliations
                [1 ]School of Marine Sciences, University of Maine, Orono, Maine, United States of America
                [2 ]Department of Structural Biology, Weizmann Institute of Science, Rehovot, Israel
                [3 ]Department of Physiology and Cell Biology, Ben-Gurion University, Beer-Sheva, Israel
                University of Ottawa, Canada
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LKB RG IR. Performed the experiments: LKB RG IR. Analyzed the data: LKB RG IR. Contributed reagents/materials/analysis tools: LKB RG IR. Wrote the paper: LKB RG IR.

                Article
                PONE-D-14-31251
                10.1371/journal.pone.0109089
                4206279
                25337801
                cb878798-1d8c-4677-a93f-ad1aefb670e2
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 July 2014
                : 8 September 2014
                Page count
                Pages: 7
                Funding
                This work was supported by the USA National Science Foundation NSF0724744. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biomechanics
                Marine Biology
                Phycology
                Plant Science
                Earth Sciences
                Marine and Aquatic Sciences
                Oceanography
                Biological Oceanography
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper.

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