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      Surface chemical defence of the eelgrass Zostera marina against microbial foulers

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          Abstract

          Plants rely on both mechanical and chemical defence mechanisms to protect their surfaces against microorganisms. The recently completed genome of the eelgrass Zostera marina, a marine angiosperm with fundamental importance for coastal ecosystems, showed that its re-adaptation from land to the sea has led to the loss of essential genes (for chemical communication and defence) and structural features (stomata and thick cuticle) that are typical of terrestrial plants. This study was designed to understand the molecular nature of surface protection and fouling-control strategy of eelgrass against marine epiphytic yeasts. Different surface extraction methods and comparative metabolomics by tandem mass spectrometry (LC-MS/MS) were used for targeted and untargeted identification of the metabolite profiles of the leaf surface and the whole tissue extracts. Desorption electrospray ionization-imaging mass spectrometry (DESI-IMS) coupled with traditional bioassays revealed, for the first time, the unique spatial distribution of the eelgrass surface-associated phenolics and fatty acids, as well as their differential bioactivity against the growth and settlement of epiphytic yeasts. This study provides insights into the complex chemical defence system of the eelgrass leaf surface. It suggests that surface-associated metabolites modulate biotic interactions and provide chemical defence and structural protection to eelgrass in its marine environment.

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          Mass spectral molecular networking of living microbial colonies.

          Integrating the governing chemistry with the genomics and phenotypes of microbial colonies has been a "holy grail" in microbiology. This work describes a highly sensitive, broadly applicable, and cost-effective approach that allows metabolic profiling of live microbial colonies directly from a Petri dish without any sample preparation. Nanospray desorption electrospray ionization mass spectrometry (MS), combined with alignment of MS data and molecular networking, enabled monitoring of metabolite production from live microbial colonies from diverse bacterial genera, including Bacillus subtilis, Streptomyces coelicolor, Mycobacterium smegmatis, and Pseudomonas aeruginosa. This work demonstrates that, by using these tools to visualize small molecular changes within bacterial interactions, insights can be gained into bacterial developmental processes as a result of the improved organization of MS/MS data. To validate this experimental platform, metabolic profiling was performed on Pseudomonas sp. SH-C52, which protects sugar beet plants from infections by specific soil-borne fungi [R. Mendes et al. (2011) Science 332:1097-1100]. The antifungal effect of strain SH-C52 was attributed to thanamycin, a predicted lipopeptide encoded by a nonribosomal peptide synthetase gene cluster. Our technology, in combination with our recently developed peptidogenomics strategy, enabled the detection and partial characterization of thanamycin and showed that it is a monochlorinated lipopeptide that belongs to the syringomycin family of antifungal agents. In conclusion, the platform presented here provides a significant advancement in our ability to understand the spatiotemporal dynamics of metabolite production in live microbial colonies and communities.
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            Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress.

            Osmolytes are low-molecular-weight organic solutes, a broad group that encompasses a variety of compounds such as amino acids, tertiary sulphonium and quaternary ammonium compounds, sugars and polyhydric alcohols. Osmolytes are accumulated in the cytoplasm of halophytic species in order to balance the osmotic potential of the Na(+) and Cl(-) accumulated in the vacuole. The advantages of the accumulation of osmolytes are that they keep the main physiological functions of the cell active, the induction of their biosynthesis is controlled by environmental cues, and they can be synthesized at all developmental stages. In addition to their role in osmoregulation, osmolytes have crucial functions in protecting subcellular structures and in scavenging reactive oxygen species.
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              The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea.

              Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.
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                Author and article information

                Contributors
                dtasdemir@geomar.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                26 February 2019
                26 February 2019
                2019
                : 9
                : 3323
                Affiliations
                [1 ]ISNI 0000 0000 9056 9663, GRID grid.15649.3f, GEOMAR Centre for Marine Biotechnology, Research Unit Marine Natural Products Chemistry, GEOMAR Helmholtz Centre for Ocean Research Kiel, ; Am Kiel Kanal 44, 24106 Kiel, Germany
                [2 ]ISNI 0000 0000 9056 9663, GRID grid.15649.3f, Research Unit Marine Benthic Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, ; Düsternbrooker Weg 20, 24105 Kiel, Germany
                [3 ]ISNI 0000 0001 2153 9986, GRID grid.9764.c, Kiel University, ; Christian-Albrechts-Platz 4, 24118 Kiel, Germany
                Article
                39212
                10.1038/s41598-019-39212-3
                6389981
                30804483
                79aa2f25-6a1f-411c-aff6-464cdacdc2a7
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 26 October 2018
                : 17 January 2019
                Funding
                Funded by: Stiftelsen Blanceflor Boncompagni Ludovisi scholarship for 6 months
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