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Seagrass-mediated phosphorus and iron solubilisation in tropical sediments Kasper Elgetti Brodersen, Klaus Koren, Maria Mosshammer, Peter Ralph, Michael Kühl, and Jakob Santner Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03878 • Publication Date (Web): 17 Nov 2017 Downloaded from http://pubs.acs.org on November 18, 2017
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Seagrass-mediated phosphorus and iron solubilisation in tropical sediments Kasper Elgetti Brodersen1,2,*, Klaus Koren2,*, Maria Moßhammer2,*, Peter J. Ralph1, Michael Kühl1,2,#, Jakob Santner3,4,#
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1
Climate Change Cluster, Faculty of Science, University of Technology Sydney (UTS), Sydney, Australia. 2
Marine Biological Section, Department of Biology, University of Copenhagen, Helsingør, Denmark. 3
Division of Agronomy, Department of Crop Sciences, University of Natural Resources and Life Sciences, Vienna, Austria. 4
Rhizosphere Ecology and Biogeochemistry Group, Institute of Soil Research, Department of Forest and Soil Sciences, University of Natural Resources and Life Sciences, Vienna, Austria.
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*
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#
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These authors contributed equally to this work and share the first authorship of this paper
Corresponding authors:
[email protected] (Michael Kühl) and
[email protected] (Jakob Santner)
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Summary: Seagrasses can modulate their rhizosphere microenvironment to enhance phosphorus and iron availability in carbonate-rich sediments, which explains how seagrasses can thrive in oligotrophic tropical waters.
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Running title: Seagrass nutrient mobilization
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Word count:
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Abstract: 159 words. Main text: 3.114 words. Figures: 5 (multi-panel figures).
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ABSTRACT
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Tropical seagrasses are nutrient limited owing to the strong phosphorus fixation capacity of
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carbonate-rich sediments, yet they form densely-vegetated, multi-species meadows in
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oligotrophic tropical waters. Using a novel combination of high-resolution, two-dimensional
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chemical imaging of O2, pH, iron, sulphide, calcium and phosphorus, we found that tropical
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seagrasses are able to mobilize the essential nutrients iron and phosphorus in their
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rhizosphere via multiple biogeochemical pathways. We show that tropical seagrasses
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mobilize phosphorus and iron within their rhizosphere via plant-induced local acidification,
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leading to dissolution of carbonates and release of phosphate, and via local stimulation of
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microbial sulphide production, causing reduction of insoluble Fe(III) oxyhydroxides to
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dissolved Fe(II) with concomitant phosphate release into the rhizosphere porewater. These
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nutrient mobilization mechanisms have a direct link to seagrass-derived radial O2 loss and
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secretion of dissolved organic carbon from the below-ground tissue into the rhizosphere.
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Our demonstration of seagrass-derived rhizospheric phosphorus and iron mobilization
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explains why seagrasses are widely distributed in oligotrophic tropical waters.
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Keywords: carbonate, chemical imaging, in situ, iron, pH, phosphorus, seagrass, sediment, solubilisation, sulphide
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INTRODUCTION
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Seagrasses are found in coastal waters worldwide except Antarctica, and seagrass meadows
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are important high-value ecosystems1,2 providing numerous ecosystem services in terms of
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high biodiversity,3 enhanced sediment carbon sequestration,4 and coastal zone protection
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against erosion.5 In tropical sedimentary environments, strong fixation of phosphorus in the
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prevailing carbonate-rich sediments6-9 and adsorption of phosphorus to insoluble
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iron(Fe)(III) oxyhydroxides10 lead to strong nutrient limitation. Phosphorus deficiency can
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negatively affect numerous plant processes such as energy transfer, photosynthesis,
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respiration, enzyme regulation, and the synthesis of nucleic acids and membranes.11
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Phosphorus is mainly absorbed through the rhizome and roots of seagrasses,12 and despite
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very low (nM) free phosphorus levels in pore waters of carbonate-rich sediments in
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oligotrophic waters, seagrasses thrive and sustain high primary production forming
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extensive meadows in such tropical habitats.13 Seagrasses growing in carbonate-rich
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sediments also suffer from Fe deficiency14 with potentially adverse effects on photopigment
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concentrations in leaves. Tropical seagrass species such as Cymodocea sp., Halodule sp.,
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Halophila sp., and Thalassia sp. thus seem to have evolved phosphorus, and possibly iron,
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acquisition mechanisms to support their nutrient requirements, but experimental
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demonstration of plant-mediated nutrient mobilization from sediments is hitherto lacking.15
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It has been suggested, that seagrass-generated rhizospheric phosphorus solubilisation is
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linked to i) the release of organic acids from roots (or organic acids derived by fermentation
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of root/rhizome exudates, such as sucrose),16 and ii)
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rhizosphere pH as a result of root/rhizome-released acidic substances and/or radial O2 loss
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(ROL), which leads to acidification through the oxidation of sediment-produced sulphide.17,18
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Such rhizosphere acidification may result in carbonate dissolution and concomitant
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phosphate release into the porewater. Seagrasses mainly leak O2 from the root/shoot
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junctions and the root apical meristem area close to the root-tips,17,19,20 whereas mature
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parts of the roots possess barriers to ROL.21 Barriers to ROL likely improve the efficiency of
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long-distance gas transport within the aerenchyma and thereby improve the internal plant
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aeration.22 The rate of ROL from the below-ground tissue is thus largely determined by the
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internal O2 concentration gradient, where the leaves functions as O2 source and the below-
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ground tissue as O2 sink.23 ROL from the below-ground tissue is higher during active leaf
plant-derived decreases of the
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photosynthesis as compared to during night-time where seagrasses depend on the O2
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availability in the ambient water.17,19,24
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Seagrasses also secrete dissolved organic carbon (DOC) into their rhizosphere as
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root/rhizome exudates,25 which fuel the rhizospheric microbial community,26 and have been
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shown to stimulate N2 fixation in the seagrass rhizosphere via sulphate-reducing
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diazotrophs, thus relieving nitrogen limitation.27 Sulphate-reducing bacteria (SRB) are highly
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abundant in seagrass-inhabited sediments,28,29 where sulphate reduction rates have been
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shown to increase during photosynthesis.30,31 SRB form hydrogen sulphide (H2S), which is
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toxic to seagrasses.32 H2S intrusion into the below-ground aerenchymal tissue has previously
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been reported, especially during unfavourable environmental conditions such as water-
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column hypoxia, high water-column turbidity, and sedimentation onto seagrass leaves
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impeding the internal plant aeration.33,34 The ability of seagrasses to aerate the rhizosphere
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and alter the rhizospheric biogeochemical processes and geochemical conditions is thus
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critical for their survival. SRB may play multiple roles in tropical sediments. It has been
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proposed that high rhizospheric H2S concentrations can reduce insoluble Fe(III)
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oxyhydroxides to dissolved Fe(II), co-dissolving Fe(III) oxyhydroxide-bound phosphate,10 in
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addition to the positive effect that N2-fixing SRB appear to have on the porewater nitrogen
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availability. In this way, SRB may have both beneficial and detrimental effects on seagrass
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health. Moreover, root/rhizome exudates may also directly stimulate microbiological Fe(III)
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reduction, thus further supporting the seagrasses’ Fe demand. However, the mentioned
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plant-mediated phosphorus and iron mobilization mechanisms remain speculative and have
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never been demonstrated directly in the seagrass rhizosphere.
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Using a novel combination of high-resolution in situ chemical imaging methods (see detailed
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description in the Supporting Information; notes S1; fig. S1-S6), we now present the first
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experimental demonstration of seagrass-derived rhizospheric phosphorus and iron
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mobilization, thus resolving how tropical seagrasses thrive in nutrient-poor carbonate
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sediments. The underlying hypotheses were (i) that seagrasses can actively stimulate
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sulphide production in the rhizosphere leading to reduction of insoluble Fe(III)
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oxyhydroxides to Fe(II), and (ii) that local acidification of the rhizosphere via ROL (potentially
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supported by Fe(II) oxidation) results in concomitant dissolution of carbonates and thus
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releases sediment-bound phosphorus to the porewater. Moreover, diel cycles of ROL may 5 ACS Paragon Plus Environment
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favour microbiological Fe(III) and sulphate reduction in the night, and chemical and
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microbiological Fe(II) and sulphide oxidation, and thus rhizospheric acidification during the
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day; thereby, representing a shift in P sources over a diurnal cycle.
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MATERIALS AND METHODS
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Experimental setup and study site
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Seagrass specimens of Cymodocea serrulata (R.Br.) Asch. & Magnus and carbonate-rich,
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tropical marine sediment were collected at Green Island, Cairns, Australia (16° 45’ 26.244”
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S; 145° 58’ 25.7376” E). Prior to experiments, the sediment was sieved to obtain the
