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Effects of Cyclic Hypoxia on Gene Expression and Reproduction in a Grass Shrimp, Palaemonetes pugio

Nancy J. Brown-Peterson¹, C. Steve Manning¹, Vishal Patel^2,*, Nancy D. Denslow² and Marius Brouwer^1,

¹ Department of Coastal Sciences, The University of Southern Mississippi, 703 East Beach Dr., Ocean Springs, Mississippi 39564
² Department of Physiological Sciences and Center for Environmental and Human Toxicology, University of Florida, PO Box 110885, Gainesville, Florida 32611

To whom correspondence should be addressed. E-mail: marius.brouwer{at}usm.edu

Cyclic changes in dissolved oxygen occur naturally in shallow estuarine systems, yet little is known about the adaptations and responses of estuarine organisms to cyclic hypoxia. Here we examine the responses of Palaemonetes pugio, a species of grass shrimp, to cyclic hypoxia (1.5–8 mg/l dissolved oxygen; 4.20–22.42 kPa) at both the molecular and organismal levels. We measured alterations in gene expression in hepatopancreas tissue of female grass shrimp using custom cDNA macroarrays. After short-term (3-d) exposure to cyclic hypoxia, mitochondrial manganese superoxide dismutase (MnSOD) was upregulated and 70-kd heat shock proteins (HSP70) were downregulated. After 7-d exposure, nuclear genes encoding mitochondrial proteins (ribosomal protein S2, ATP synthase, very-long-chain specific acyl-CoA dehydrogenase [VLCAD]) were downregulated, whereas mitochondrial phosphoenol pyruvate carboxykinase (PEP Cbk) was upregulated. After 14 d, vitellogenin and apolipoprotein A1 were upregulated. Taken together, these changes suggest a shift in metabolism toward gluconeogenesis and lipid export. Long-term (77-d) exposure to hypoxia showed that profiles of gene expression returned to pre-exposure levels. These molecular responses differ markedly from those induced by chronic hypoxia. At the organismal level, cyclic hypoxia reduces the number of broods and eggs a female can produce. Demographic analysis showed a lower estimated rate of population growth in grass shrimp exposed to both continuous and short-term cyclic hypoxia, suggesting population-level impacts on grass shrimp.

Abbreviations: DO, dissolved oxygen • HH, continuous exposure to cyclic hypoxia • HN, 2-week exposure to cyclic hypoxia and then exposure to normoxia • NN, continuous exposure to normoxia • PEP Cbk, phosphoenol pyruvate carboxykinase • SAM, significance analysis of microarrays • SOD, superoxide dismutase • VLCAD, very-long-chain specific acyl-CoA dehydrogenase