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First published online June 15, 2007
Journal of Experimental Biology 210, 2253-2266 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005116
Extreme anoxia tolerance in embryos of the annual killifish Austrofundulus limnaeus: insights from a metabolomics analysis
1 Department of Biology, Portland State University, PO Box 751, Portland, OR
97207-0751, USA
2 Department of Neurobiology, Pharmacology, and Physiology, The University
of Chicago, Chicago, IL 60637, USA
3 Department of Chemistry, Belknap Research Building, 2210 S. Brook Street,
University of Louisville, Louisville, KY 40208, USA
4 Hopkins Marine Station, Stanford University, Oceanview Boulevard, Pacific
Grove, CA 93950, USA
* Author for correspondence (e-mail: jpod{at}pdx.edu)
Accepted 5 April 2007
The annual killifish Austrofundulus limnaeus survives in ephemeral
pond habitats by producing drought-tolerant diapausing embryos. These embryos
probably experience oxygen deprivation as part of their normal developmental
environment. We assessed the anoxia tolerance of A. limnaeus embryos
across the duration of embryonic development. Embryos develop a substantial
tolerance to anoxia during early development, which peaks during diapause II.
This extreme tolerance of anoxia is retained during the first 4 days of
post-diapause II development and is then lost. Metabolism during anoxia
appears to be supported mainly by production of lactate, with alanine and
succinate production contributing to a lesser degree. Anoxic embryos also
accumulate large quantities of
-aminobutyrate (GABA), a potential
protector of neural function. It appears that the suite of characters
associated with normal development and entry into diapause II in this species
prepares the embryos for long-term survival in anoxia even while the embryos
are exposed to aerobic conditions. This is the first report of such extreme
anoxia tolerance in a vertebrate embryo, and introduces a new model for the
study of anoxia tolerance in vertebrates.
Key words: anaerobiosis, anoxia, development, fish, GABA, lactate, metabolic depression
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