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Effects of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum

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Abstract

Dinoflagellate algae of the genus Symbiodinium occur as endosymbionts in a variety of hosts including coral. The response of Symbiodinium spp. to environmental changes could dictate survival of their hosts and the ecological success of coral reef ecosystems. Oxidative stress has been linked to a breakdown in this symbiotic relationship, known as bleaching. Increased temperature is one of the primary environmental changes linked to this phenomenon. Preliminary studies have established high concentrations of the sulfur compound dimethylsulfoniopropionate (DMSP) in Symbiodinium spp., with increased temperature. To examine the potential use of DMSP as an antioxidant, a 5 day incubation experiment was conducted at two temperatures with the algae S. microadriaticum (CCMP1633) isolated from the cnidarian host Aiptasia pulchella. An HPLC assay for the activity of the enzyme B12-dependent methionine synthase was modified and used to determine the link between de novo production of methionine, a precursor to DMSP, and temperature induced oxidative stress. DMSP concentrations per cell increased approximately 38 % in the 33 °C treatment cultures over 120 h. However, these cells also increased more than 2-fold in biovolume (127 ± 43 %), and SYTO-BC stain indicated increased DNA content (approximately 4-fold), suggesting arrested cell division. Normalization of DMSP to biovolume revealed that the concentrations actually decreased approximately 49 % after 2 days in cultures exposed to elevated temperature (33 °C), but were not significantly different from the control treatment at 120 h (27 °C). Concomitant changes in the 33 °C treatment relative to the control (after 120 h) resulted in an approximately 8-fold increase in reactive oxygen species, a 37 % (±7 %) decrease in photosynthetic efficiency of photosystem II, and a 5-fold increase in xanthophyll cycling. Methionine synthase activity (MSA) correlated to the decrease in DMSP concentration (R 2 = 0.778), with decreasing activity at the high temperature. Given this decrease in MSA, the increase in DMSP per cell may be due to DMSP production utilizing methionine from protein turnover, and not de novo synthesis via MSA. The findings of this study provide insight into the responses of algal symbionts to environmental changes, shed light on the potential use of DMSP and other known photo-protective mechanisms such as xanthophyll cycling under temperature induced oxidative stress, and support the suspected cessation of cell division under these conditions. This information could be crucial to understanding cellular responses to environmental changes and the ability of these organisms to survive under elevated sea surface temperatures projected for the near future.

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Acknowledgments

This research was conducted at Hollings Marine Laboratory, Charleston, SC, and was funded by various National Science Foundation/Ocean Sciences grants (Dr. Giacomo DiTullio: OCE-0728683, OCE-0338097, NSF-ANT-0739597, and Dr. Mike Janech : NSF-ANT-0739446). We are extremely appreciative of Dr. Michael Janech for his integral role in this research. We express gratitude to Dr. Peter Moeller for the use of his facilities, to Kevin Huncik for technical assistance, and to Jennifer Bennett, Dr. Peter Lee, Tyler Cyronak, Barbara Lyon, Juliana Miller, Sarah Riseman, and Dr. Erik Sotka for their comments and suggestions. This contribution represents No. 384 to the Grice Marine Laboratory, Charleston, SC.

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  1. Hollings Marine Laboratory, College of Charleston, 205 Fort Johnson, Charleston, SC, 29412, USA

    Amanda L. McLenon & Giacomo R. DiTullio

  2. Grice Marine Laboratory, College of Charleston, 205 Fort Johnson, Charleston, SC, 29412, USA

    Giacomo R. DiTullio

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  1. Amanda L. McLenon
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Correspondence to Amanda L. McLenon.

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McLenon, A.L., DiTullio, G.R. Effects of increased temperature on dimethylsulfoniopropionate (DMSP) concentration and methionine synthase activity in Symbiodinium microadriaticum . Biogeochemistry 110, 17–29 (2012). https://doi.org/10.1007/s10533-012-9733-0

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