Trace Gas Biogeochemistry
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The forgotten hormone:
Is ethene (ethylene) co-produced with DMS in marine algae?

by Ina Plettner and Michael Steinke email

 

(Also see general section on Non-Methane Hydrocarbons)

 

Principal investigators: Michael Steinke and Gill Malin
Senior Research Associate: Ina Plettner
Funding: UK Natural Environment Research Council (NER/M/S/2002/00122) November 2002 - October 2003


Introduction

Hormones are chemical messengers (infochemicals) in living organisms. For example, release of the hormone adrenaline into the arteries of humans effects the mobilisation of sugars and fats and results in a general increase in metabolic rate. Ethene (ethylene; H2C=CH2) is the only gaseous plant hormone produced during all stages of plant growth. It is also part of a signalling system in plant responses to light, including harmful ultraviolet (UV-B) radiation (Mackerness 2000). Often ethene is produced during and after stress such as mechanical damage or extreme temperatures.

Marine ecosystems are also a source of ethene (Figure 1) where it is produced both photochemically, as a by-product of organic matter degradation, and through biological processes. However, very little is known about its direct production by marine organisms such as seaweeds or phytoplankton. The atmosphere is an important sink for ethene produced in marine or freshwater systems. Because of its high reactivity towards hydroxyl (OH) radicals, ethene plays a significant role in tropospheric chemistry and the production of ozone. This contribution to atmospheric chemistry makes ethene a climate-relevant trace gas and its production pathways are of interest to both, marine and atmospheric scientists.

Figure 1 - Ethene in the natural environment


Metabolic pathways of ethene synthesis

The major route of ethene synthesis in higher plants involves the following metabolic sequence: methionine is converted with ATP to adenosylmethionine (AdoMet) which is then catalysed to aminocyclopropane carboxylic acid (ACC) via the enzyme ACC synthase. The final reaction, the oxidation of ACC through the enzyme ACC oxidase, results in the production of ethene (Figure 2).

Figure 2 - Pathways for ethene production in higher plants (top) and suggested route for ethene synthesis in some marine algae (bottom)


Maillard et al. (1993) demonstrated this production pathway in the freshwater greenalgae Haematococcus pluvialis, but cofactor requirements in this unicellular species were different to those of higher plants, suggesting that additional alternative pathways are likely to exist. One such alternative route is the production of ethene from acrylate (e.g., Abeles 1973, Watanabe & Kondo 1976; Figure 2). In some marine algae, acrylate can be produced from the secondary metabolite dimethylsulphoniopropionate (DMSP) in an enzymatic reaction that produces the volatile trace gas dimethyl sulphide (DMS). The enzyme required for acrylate formation, DMSP lyase, has been identified in several algal taxa including benthic macroalgae and pelagic phytoplankton (Stefels & van Boekel 1993, Steinke et al. 1996, Steinke et al. 1998).

The production of ethene from acrylate involves the equimolar release of CO2 and requires the presence of acrylate decarboxylase, an enzyme previously purified from the wax bean Phaseolus vulgaris (Ghooprassert and Spencer 1975) and yeast (Shimokawa and Kasai 1970). Provided that this enzyme is present in marine algae, the production of the climate relevant trace gases DMS and ethene could be linked in marine algae, as outlined in Figure 2.


Current research

Field data indicate that ethene production may be linked with the enzymatic cleavage of DMSP to equimolar quantities of acrylate and DMS. In our project, we focus on the possible effects of light-stress on ethene and DMS production (Figure 3) and investigate whether acrylate can be a direct precursor for ethene production in marine algae. The physiological response of algae to increased ethene concentrations is of additional interest. In higher plants, elevated ethene concentrations result in chlorophyll degradation and synthesis of protective pigments including carotenes. Whether marine algae use ethene as a hormone to regulate their physiological response to light stress is possible but currently unknown. Our preliminary experiments indicate changes in the relative pigment composition of marine phytoplankton after exposure to ethene.

Of further interest is the possible role of ethene as an infochemical in marine trophic interactions. Analogous to gaseous "trophochemcials" in higher plants that are produced after attack by a herbivore, these infochemicals may be involved in shaping the structure and functioning of marine food webs.

Figure 3 - High light intensities may result in increased conversion of dimethylsulphoniopropionate (DMSP) to acrylate and dimethyl sulphide (DMS). It is likely that DMS can scavenge harmful reactive oxygen species via oxidation to dimethylsulphoxide (DMSO). The production of ethene from acrylate is still hypothetical for marine algae


Literature

  • Abeles, F.B. 1973. Ethylene in Plant Biology. Academic Press, New York.
  • Mackerness, S.A.H. 2000. Plant responses to ultraviolet-B (UV-B: 280-320 nm) stress: What are the key regulators? Plant Growth Regulation 32: 27-39.
  • Maillard, P., C. Thepenier, and C. Gudin. 1993. Determination of an ethylene biosynthesis pathway in the unicellular green alga, Haematococcus pluvialis. Relationship between growth and ethylene production. Journal of Applied Phycology 5: 93-98.
  • Ghooprasert, P. and M. Spencer. 1975. Preparation and purification of an enzyme system for ethylene synthesis from acrylate. Physiologie Vegetale 13: 579-589.
  • Shimokawa, K. and Z. Kasai. 1970. Ethylene formation from acrylic acid by a banana pulp extract. Agricultural and Biological Chemistry 34: 1646-1651.
  • Stefels, J. and W. H. M. van Boekel. 1993. Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Marine Ecology - Progress Series 97: 11-18.
  • Steinke, M., C. Daniel, and G. O. Kirst. 1996. DMSP Lyase in marine macro- and microalgae: Intraspecific differences in cleavage activity. In: Biological and Environmental Chemistry of DMSP and Related Sulfonium Compounds, edited by R. P. Kiene, P. T. Visscher, M. D. Keller, and G. O. Kirst. Plenum Press, New York, p. 317-324.
  • Steinke, M., G. V. Wolfe, and G. O. Kirst. 1998. Partial characterisation of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Marine Ecology - Progress Series 175: 215-225.
  • Watanabe, T. and N. Kondo. 1976. Ethylene evolution in marine algae and a proteinaceous inhibitor of ethylene biosynthesis from red alga. Plant and Cell Physiology 17: 1159-1166.