GABA metabolism is crucial for long-term survival of anoxia in annual killifish embryos

Author:

Zajic Daniel E.12ORCID,Podrabsky Jason E.1ORCID

Affiliation:

1. Department of Biology, Portland State University, P.O. Box 751, Portland, OR 97207, USA

2. Health, Human Performance, and Athletics Department, Linfield University, 900 SE Baker, McMinnville, OR 97128, USA

Abstract

In most vertebrates, a lack of oxygen quickly leads to irreparable damages to vital organs, such as the brain and heart. However, there are some vertebrates that have evolved mechanisms to survive periods of no oxygen (anoxia). The annual killifish (Austrofundulus limnaeus) survives in ephemeral ponds in the coastal deserts of Venezuela and their embryos have the remarkable ability to tolerate anoxia for months. When exposed to anoxia, embryos of A. limnaeus respond by producing significant amounts of γ-aminobutyric acid (GABA). This study aims to understand the role of GABA in supporting the metabolic response to anoxia. To explore this, we investigated four developmentally distinct stages of A. limnaeus embryos that vary in their anoxia tolerance. We measured GABA and lactate concentrations across development in response to anoxia and aerobic recovery. We then inhibited enzymes responsible for the production and degradation of GABA and observed GABA and lactate concentrations, as well as embryo mortality. Here, we show for the first time that GABA metabolism affects anoxia tolerance in A. limnaeus embryos. Inhibition of enzymes responsible for GABA production (glutamate decarboxylase) and degradation (GABA-transaminase and succinic acid semialdehyde dehydrogenase) led to decreased mortality, supporting a role for GABA as an intermediate product and not a metabolic end product. We propose multiple roles for GABA during anoxia and aerobic recovery in A. limnaeus embryos, serving as a neurotransmitter, an energy source, and an antioxidant.

Funder

National Science Foundation

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

Cited by 6 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. GABAergic Mechanisms of the Brain Tolerance to Hypoxia in Lower Vertebrates;Российский физиологический журнал им  И  М  Сеченова;2023-04-01

2. GABAergic Mechanisms of Brain Tolerance to Hypoxia in Lower Vertebrates;Journal of Evolutionary Biochemistry and Physiology;2023-03

3. Stress, membraneless organelles, and liquid–liquid phase separation;Droplets of Life;2023

4. Fipronil impairs the GABAergic brain responses of Nile Tilapia during the transition from normoxia to acute hypoxia;Journal of Experimental Zoology Part A: Ecological and Integrative Physiology;2022-10-10

5. Review: A history and perspective of mitochondria in the context of anoxia tolerance;Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology;2022-06

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