Seagrasses actively modify their below-ground geochemical microenvironment: a microsensor study of Zostera muelleri

Kasper Elgetti Brodersen1, Daniel A. Nielsen1, Peter J. Ralph1 and Michael Kühl1,2

1 Plant Functional Biology and Climate Change Cluster, University of Technology, Sydney, Australia

2 Marine Biological Section, University of Copenhagen, Denmark

• Seagrass meadows constitute globally important marine

ecosystems; supporting high marine biodiversity and protecting

coastal areas from erosion.

• Over the past century, the worldwide extent of seagrass meadows

have declined with an alarming rate, and in order to better manage

these vital marine habitats for long-term preservation, new insight

into the possible geochemical mechanisms behind these die-

backs is crucial.

Tissue

Skeleton

a b

1 cm

• Electrochemical microsensors and planar optodes were used in

combination with a custom-made split flow-chamber with artificial,

transparent sediment, to investigate the below-ground chemical

microenvironment of Zostera muelleri ssp. capricorni under

changing environmental conditions.

500 µm 1 mm

a b c

Fig. 2 Experimental setup. Microsensor positioning and data acquisition was achieved via

dedicated PC software (SensorTracePro, Unisense A/S; VisiSens, PreSens).

Acknowledgements: We thank Ole Pedersen, Jens Borum, Verena Schrameyer, Milan Szabo and Mathieu Pernice. This project was funded by the Australian Research Council (ARC) and the Danish Council for Independent Research | Natural sciences.

Corresponding author: kasper.e.brodersen@student.uts.edu.au

Publications: Brodersen et al. 2014. A split flow-chamber with artificial sediment to examine the below-ground microenvironment of aquatic macrophytes. Marine Biology DOI: 10.1007/s00227-014-2542-3

Brodersen et al. 2014. Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide. New Phytologist DOI: 10.1111/nph.13124

Seagrass illustration in Fig 1 and 6 originates from the IAN image library: Diana Kleine, Integration and Application Network, University of Maryland, Center for Environmental Science (ian.umces.edu/imagelibrary/).

Fig. 5 Two-dimensional O2 image of actively growing Z. muelleri roots (colour coded). The O2

distribution was determined during a light-dark transition. Legend depicts the O2 concentration in

% air saturation.

b

• Oxic microshield & local pH enhancement provide protection

against sediment-produced reduced phytotoxins, such as H2S.

• During water-column hypoxia, the oxic microzone around the

meristematic tissue was significantly reduced, resulting in high

levels of H2S reaching the tissue surface and a concomitant

decrease in the plants overall viability

Fig. 3 Dynamics of the below-ground chemical microenvironment determined during light-dark

transitions, as well as during an over-night water-column hypoxia event. Legend depicts the

different experimentally manipulated treatments (light intensity in µE m-2 s-1). Y-axis = 0 indicate

the below-ground tissue surface. n=3.

Background

Materials & Methods

Results: Chemical microenvironment

Conclusion: Chemical

defence mechanism revealed

Aim & Hypothesis

• Can seagrasses actively alter their below-ground biogeochemical

microenvironment through the release of chemical compounds?

• Seagrasses actively alter their below-ground geochemical

microenvironment through the release of chemical compounds,

such as O2, and thereby accommodate their own growth.

Fig. 6 Conceptual diagram visualising the major findings of the present study. Hence, a local oxic

microzone around the root-shoot junctions protecting the active parts of the below-ground

tissue from reduced, toxic compounds produced in the surrounding sediment through microbial

metabolisms.

Fig. 7 Cross tissue sections from the basal meristem region. (a) Protecting (external) oxic

microshield present. (b) Inadequate internal aeration may lead to sulphide intrusion.

• Actively growing roots leak O2 from around the apical root

meristem, thereby oxidizing the surrounding below-ground

microenvironment, as they grow through the reduced sediment.

Fig. 1 Conceptual diagram illustrating the biogeochemical processes of Zostera muelleri spp.

capricorni. Passive (night-time) or actively (day-time) evolved O2 is transported down to the below-

ground tissue through low-resistance internal gas channels (i.e. the aerenchyma) and is

subsequently lost to the immediate rhizosphere. Thus potentially providing protection against

sediment-produced reduced, phytotoxic compounds.

Below-ground geochemical microenvironment

• Z. muelleri can thus protect itself against phytotoxic H2S by

modifying its below-ground geochemical microenvironment through

the release of chemical compounds, a vital chemical defence

mechanism that becomes highly inefficient during over-night water-

column hypoxia.

• Radial O2 loss from the basal meristem with leaf sheath lead to the

formation of a ~300 µm wide oxic microzone around the

meristematic tissue, wherein no (or very low levels of) H2S could

be observed at the tissue surface despite high concentrations in

the surrounding artificial sediment (i.e. >200 µmol H2S L-1).

• A significant decrease in pH within the oxic microzone was also

detected which could play an important role in the release of

sediment-bound phosphorus in natural systems.

Fig. 4 Microelectrode measurements towards the below-ground tissue surface (at y-axis = 0)

visualising the protecting oxic microshield and a concomitant decrease in pH and H2S. The latter

was most likely due to the formation of sulphuric acid produced via the chemical reaction between

plant-mediated O2 and sediment-produced H2S. n=3

2D O2 microdistribution

Oxic microshield

Chemical defence mechanism