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Title: Surface chemical defence of the eelgrass Zostera marina against microbial foulers

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.

Authors:
 [1];  [1];  [2];  [2];  [1]
  1. GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel (Germany). GEOMAR Centre for Marine Biotechnology, Research Unit Marine Natural Products Chemistry
  2. GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel (Germany). Research Unit Marine Benthic Ecology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
Sponsoring Org.:
USDOE
OSTI Identifier:
1542435
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 9; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Papazian, Stefano, Parrot, Delphine, Burýšková, Barbora, Weinberger, Florian, and Tasdemir, Deniz. Surface chemical defence of the eelgrass Zostera marina against microbial foulers. United States: N. p., 2019. Web. doi:10.1038/s41598-019-39212-3.
Papazian, Stefano, Parrot, Delphine, Burýšková, Barbora, Weinberger, Florian, & Tasdemir, Deniz. Surface chemical defence of the eelgrass Zostera marina against microbial foulers. United States. doi:10.1038/s41598-019-39212-3.
Papazian, Stefano, Parrot, Delphine, Burýšková, Barbora, Weinberger, Florian, and Tasdemir, Deniz. Tue . "Surface chemical defence of the eelgrass Zostera marina against microbial foulers". United States. doi:10.1038/s41598-019-39212-3. https://www.osti.gov/servlets/purl/1542435.
@article{osti_1542435,
title = {Surface chemical defence of the eelgrass Zostera marina against microbial foulers},
author = {Papazian, Stefano and Parrot, Delphine and Burýšková, Barbora and Weinberger, Florian and Tasdemir, Deniz},
abstractNote = {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.},
doi = {10.1038/s41598-019-39212-3},
journal = {Scientific Reports},
number = 1,
volume = 9,
place = {United States},
year = {2019},
month = {2}
}

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Cited by: 5 works
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Figures / Tables:

Figure 1 Figure 1: Leaf tissue and surface-associated chemistry of Z. marina involved in antifouling defence. (A) Eelgrass meadow in the Baltic Sea, Kiel Fjord. Scale bar= approx. 30 cm. Photo by Stefano Papazian. (B) Cumulative regression model (Sum, purple) comparing the inhibitory antifouling activity of eelgrass extracts obtained by surface dippingmore » extraction (S, red), whole leaf (blue, W), and whole leaf after surface dipping (light-blue, W-S), on the settlement of the marine epiphytic yeast, D. hansenii. (C) Multivariate analysis (PCA 3 components) for comparative LC-MS/MS metabolomics of surface solid-phase (C18), solvent dipping (S), whole leaf (W) and surface-free (W-S) extracts. (D,E) Concentrations of phenolic metabolites detected in the (D) surface extracts (S, C18) and (E) whole leaf extracts (W, W-S), i.e. p-coumaric acid (p-Co), apigenin (A), luteolin (L), apigenin-7-sulfate (AS), luteolin-7-sulfate (LS), caffeic acid (CA), ferulic acid (FeA), rosmarinic acid (RA), zosteric acid (ZA), diosmetin (D), and diosmetin- 7-sulfate (DS). Error bars= standard error. (F) Molecular network built in GNPS from spectral data obtained from LC-MS/MS analyses of all extracts. Four main clusters show the dereplication and respective chemical groups annotated as phenolics, phospholipids, and fatty acid esters (Supplementary Table S2).« less

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Works referenced in this record:

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    Works referencing / citing this record:

    Unsaturated Fatty Acids Affect Quorum Sensing Communication System and Inhibit Motility and Biofilm Formation of Acinetobacter baumannii
    journal, January 2018

    • Nicol, Marion; Alexandre, Stéphane; Luizet, Jean-Baptiste
    • International Journal of Molecular Sciences, Vol. 19, Issue 1
    • DOI: 10.3390/ijms19010214

    Fatty acid composition of individual polar lipid classes from marine macrophytes
    journal, March 2004


    Thermotropic behaviour of membrane lipids from brown marine alga Laminaria japonica
    journal, December 2000

    • Sanina, N. M.; Kostetsky, E. Y.; Goncharova, S. N.
    • Biochemical Society Transactions, Vol. 28, Issue 6
    • DOI: 10.1042/bst0280894

    Rosmarinic Acid from Eelgrass Shows Nematicidal and Antibacterial Activities against Pine Wood Nematode and Its Carrying Bacteria
    journal, November 2012

    • Wang, Jingyu; Pan, Xueru; Han, Yi
    • Marine Drugs, Vol. 10, Issue 12
    • DOI: 10.3390/md10122729

    Chemical Ecology of Marine Angiosperms: Opportunities at the Interface of Marine and Terrestrial Systems
    journal, May 2013


    Free and bound fatty acids and hydroxy fatty acids in the living and decomposing eelgrass Zostera marina L.
    journal, August 1995


    Multiple roles for protein palmitoylation in plants
    journal, June 2008


    Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress
    journal, January 2015

    • Slama, Inès; Abdelly, Chedly; Bouchereau, Alain
    • Annals of Botany, Vol. 115, Issue 3
    • DOI: 10.1093/aob/mcu239

    Priming in Systemic Plant Immunity
    journal, April 2009


    Regulation of microbial populations by coral surface mucus and mucus-associated bacteria
    journal, September 2006


    Eelgrass Wasting Disease: Cause and Recurrence of a Marine Epidemic
    journal, December 1987

    • Short, Frederick T.; Muehlstein, Lisa K.; Porter, David
    • The Biological Bulletin, Vol. 173, Issue 3
    • DOI: 10.2307/1541701

    Phylogeographic differentiation versus transcriptomic adaptation to warm temperatures in Zostera marina , a globally important seagrass
    journal, September 2016

    • Jueterbock, A.; Franssen, S. U.; Bergmann, N.
    • Molecular Ecology, Vol. 25, Issue 21
    • DOI: 10.1111/mec.13829

    Flavonoids: Their Structure, Biosynthesis and Role in the Rhizosphere, Including Allelopathy
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    Antioxidant flavonoids and phenolic acids from leaves of Leea guineense G. Don (Leeaceae)
    journal, April 2003

    • Op de Beck, Philippe; Cartier, Gilbert; David, Bruno
    • Phytotherapy Research, Vol. 17, Issue 4
    • DOI: 10.1002/ptr.1141

    From sea to sea
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    Seaweed Allelopathy Against Coral: Surface Distribution of a Seaweed Secondary Metabolite by Imaging Mass Spectrometry
    journal, October 2012

    • Andras, Tiffany D.; Alexander, Troy S.; Gahlena, Asiri
    • Journal of Chemical Ecology, Vol. 38, Issue 10
    • DOI: 10.1007/s10886-012-0204-9

    Dissolved oxygen fluxes and ecosystem metabolism in an eelgrass ( Zostera marina ) meadow measured with the eddy correlation technique
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    • Hume, Andrew C.; Berg, Peter; McGlathery, Karen J.
    • Limnology and Oceanography, Vol. 56, Issue 1
    • DOI: 10.4319/lo.2011.56.1.0086

    The possible role of transfer cells in the adaptation of plants to salinity
    journal, August 1983


    Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study
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    • DOI: 10.1073/pnas.151258398

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    journal, October 2013

    • Rübel, Oliver; Greiner, Annette; Cholia, Shreyas
    • Analytical Chemistry, Vol. 85, Issue 21
    • DOI: 10.1021/ac402540a

    Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking
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    • Nature Biotechnology, Vol. 34, Issue 8
    • DOI: 10.1038/nbt.3597

    Antioxidant activities of polyphenols from sage (Salvia officinalis)
    journal, November 2001


    Intersection of transfer cells with phloem biology—broad evolutionary trends, function, and induction
    journal, January 2013

    • Andriunas, Felicity A.; Zhang, Hui-Ming; Xia, Xue
    • Frontiers in Plant Science, Vol. 4
    • DOI: 10.3389/fpls.2013.00221

    A comparative evaluation of biological activities and bioactive compounds of the seagrasses Zostera marina and Zostera noltei from southern Portugal
    journal, July 2015


    Short- and medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms
    journal, July 2011


    Desorption electrospray ionization mass spectrometry reveals surface-mediated antifungal chemical defense of a tropical seaweed
    journal, April 2009

    • Lane, A. L.; Nyadong, L.; Galhena, A. S.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 18
    • DOI: 10.1073/pnas.0812020106

    Metabolic reprogramming in plant innate immunity: the contributions of phenylpropanoid and oxylipin pathways
    journal, April 2004


    Chemical Defence of a Seagrass against Microfoulers and Its Seasonal Dynamics
    journal, March 2019

    • Guan, Chi; Saha, Mahasweta; Weinberger, Florian
    • Applied Sciences, Vol. 9, Issue 6
    • DOI: 10.3390/app9061258

    Mass spectral molecular networking of living microbial colonies
    journal, May 2012

    • Watrous, J.; Roach, P.; Alexandrov, T.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 26
    • DOI: 10.1073/pnas.1203689109

    Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution range
    journal, September 2011


    Debaryomyces hansenii — an extremophilic yeast with biotechnological potential
    journal, January 2006


    Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA
    journal, February 2017


    Isolation and Identification of Flavonoids Found in <i>Zostera marina</i> Collected in Norwegian Coastal Waters
    journal, January 2016

    • Enerstvedt, Kjersti Hasle; Jordheim, Monica; Andersen, Øyvind M.
    • American Journal of Plant Sciences, Vol. 07, Issue 07
    • DOI: 10.4236/ajps.2016.77111

    Distribution, structure and function of Nordic eelgrass (Zostera marina) ecosystems: implications for coastal management and conservation : DISTRIBUTION, STRUCTURE AND FUNCTION OF NORDIC SEAGRASS ECOSYSTEMS
    journal, January 2014

    • Boström, Christoffer; Baden, Susanne; Bockelmann, Anna-Christina
    • Aquatic Conservation: Marine and Freshwater Ecosystems, Vol. 24, Issue 3
    • DOI: 10.1002/aqc.2424

    Marine epibiosis. I. Fouling and antifouling: some basic aspects
    journal, January 1989


    A solid phase extraction based non-disruptive sampling technique to investigate the surface chemistry of macroalgae
    journal, January 2016


    Antimelanogenic effects of luteolin 7-sulfate isolated from Phyllospadix iwatensis Makino
    journal, June 2016

    • Kwak, J. Y.; Seok, J. K.; Suh, H. -J.
    • British Journal of Dermatology, Vol. 175, Issue 3
    • DOI: 10.1111/bjd.14496

    Sulphated Flavonoids: Biosynthesis, Structures, and Biological Activities
    journal, February 2018


    Sulfation mediates activity of zosteric acid against biofilm formation
    journal, March 2015


    A Novel Antifouling Defense Strategy from Red Seaweed: Exocytosis and Deposition of Fatty Acid Derivatives at the Cell Wall Surface
    journal, March 2016

    • Paradas, Wladimir Costa; Tavares Salgado, Leonardo; Pereira, Renato Crespo
    • Plant and Cell Physiology, Vol. 57, Issue 5
    • DOI: 10.1093/pcp/pcw039

    Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere
    journal, February 2012

    • Weston, L. A.; Ryan, P. R.; Watt, M.
    • Journal of Experimental Botany, Vol. 63, Issue 9
    • DOI: 10.1093/jxb/ers054

    The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea
    journal, January 2016

    • Olsen, Jeanine L.; Rouzé, Pierre; Verhelst, Bram
    • Nature, Vol. 530, Issue 7590
    • DOI: 10.1038/nature16548

    The Seagrass Holobiont and Its Microbiome
    journal, December 2017


    Biodiversity influences ecosystem functioning in aquatic angiosperm communities
    journal, December 2010


    Mode of action of an isolate of Candida famata in biological control of Penicillium digitatum in orange fruits
    journal, July 1996


    Imaging the Unimaginable: Desorption Electrospray Ionization – Imaging Mass Spectrometry (DESI-IMS) in Natural Product Research
    journal, January 2018

    • Parrot, Delphine; Papazian, Stefano; Foil, Daniel
    • Planta Medica, Vol. 84, Issue 09/10
    • DOI: 10.1055/s-0044-100188

    Seagrass–pathogen interactions: ‘pseudo-induction’ of turtlegrass phenolics near wasting disease lesions
    journal, November 2005

    • Steele, Lt; Caldwell, M.; Boettcher, A.
    • Marine Ecology Progress Series, Vol. 303
    • DOI: 10.3354/meps303123

    Plant–herbivore interactions in seagrass meadows
    journal, March 2006

    • Heck, Kenneth L.; Valentine, John F.
    • Journal of Experimental Marine Biology and Ecology, Vol. 330, Issue 1
    • DOI: 10.1016/j.jembe.2005.12.044

    Staring into the void: demystifying microbial metabolomics
    journal, June 2019

    • Grim, Cynthia M.; Luu, Gordon T.; Sanchez, Laura M.
    • FEMS Microbiology Letters, Vol. 366, Issue 11
    • DOI: 10.1093/femsle/fnz135

    Staring into the void: demystifying microbial metabolomics
    journal, June 2019

    • Grim, Cynthia M.; Luu, Gordon T.; Sanchez, Laura M.
    • FEMS Microbiology Letters, Vol. 366, Issue 11
    • DOI: 10.1093/femsle/fnz135

    Chemical Defence of a Seagrass against Microfoulers and Its Seasonal Dynamics
    journal, March 2019

    • Guan, Chi; Saha, Mahasweta; Weinberger, Florian
    • Applied Sciences, Vol. 9, Issue 6
    • DOI: 10.3390/app9061258

    Simulated Heatwaves Lead to Upregulated Chemical Defense of a Marine Foundation Macrophyte Against Microbial Colonizers
    journal, July 2020


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.