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Mechanisms and evolution of hypoxia tolerance in fish.

ABSTRACT: The ability of an organism to acquire O(2) from its environment is key to survival and can play an important role in dictating a species' ecological distribution. This study is the first, to our knowledge, to show a tight, phylogenetically independent correlation between hypoxia tolerance, traits involved in dictating O(2) extraction capacity and the distribution of a group of closely related fish species, sculpins from the family Cottidae, along the nearshore marine environment. Sculpins with higher hypoxia tolerance, measured as low critical O(2) tensions (P(crit)), inhabit the O2 variable intertidal zones, while species with lower hypoxia tolerance inhabit the more O(2) stable subtidal zone or freshwater. Hypoxia tolerance is phylogenetically independently associated with an enhanced O(2) extraction capacity, with three principal components accounting for 75 per cent of the variation in P(crit): routine O(2) consumption rate; mass-specific gill surface area; and whole blood haemoglobin (Hb)- O(2)-binding affinity (P(50)). Variation in whole blood Hb-O(2)P(50) is strongly correlated with the intrinsic O(2)-binding properties of the purified Hb while the differences in the concentration of the allosteric Hb modulators, ATP and GTP, provide a Hb system with substantial plasticity for survival in a highly O(2) variable environment.

SUBMITTER: Mandic M

PROVIDER: S-EPMC2660936 | biostudies-literature | 2009 Feb

REPOSITORIES: biostudies-literature

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Mechanisms and evolution of hypoxia tolerance in fish.

Mandic Milica M Todgham Anne E AE Richards Jeffrey G JG

Proceedings. Biological sciences 20090201 1657

The ability of an organism to acquire O(2) from its environment is key to survival and can play an important role in dictating a species' ecological distribution. This study is the first, to our knowledge, to show a tight, phylogenetically independent correlation between hypoxia tolerance, traits involved in dictating O(2) extraction capacity and the distribution of a group of closely related fish species, sculpins from the family Cottidae, along the nearshore marine environment. Sculpins with h ...[more]

PMID: 18996831

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Project description:Persistent hypoxic or low-oxygen conditions in aquatic systems are becoming more frequent worldwide, causing large-scale mortalities to aquatic fauna. It is poorly understood, however, whether species can acclimate to long-term hypoxic conditions. In two experiments, we exposed juvenile freshwater fish (Murray cod, Maccullochella peelii) to low-oxygen conditions and investigated acclimation effects. Experiment 1 determined how responses could be modified by exposure to different temperatures (20, 24 and 28°C) and oxygen conditions (control 6-8 mgO2 L-1 and low-oxygen 3-4 mgO2 L-1) over 30 days. Experiment 2 determined the acclimation ability of fish exposed to two temperatures (20 and 28°C) and low-oxygen conditions (3-4 mgO2 L-1) for three different acclimation periods (7, 14 and 30 days). Responses were measured by determining critical oxygen tension (P crit), loss of equilibrium and aerobic capacity using resting respirometry. In experiment 1, resting oxygen requirements were negatively affected by long-term low-oxygen exposure except at the highest temperature (28°C). However, long-term acclimation in low-oxygen improved tolerance as measured by loss of equilibrium but not P crit. In experiment 2, fish could tolerate lower oxygen levels before reaching loss of equilibrium after 7 days acclimation, but this declined overtime. Murray cod were most tolerant to low-oxygen at the lowest temperature (20°C) and shortest exposure time (7 days). Extended low-oxygen exposure resulted in reduced aerobic capacity of fish particularly at the lowest temperature. While prior exposure to low-oxygen may allow fish to cope with hypoxic conditions better in the long-term, acclimation time was inversely related to tolerance, suggesting that resistance to hypoxia might decrease as a function of exposure time. Our study fills a much-needed gap in our understanding of how freshwater species acclimate to hypoxia, and in particular, how exposure to prolonged periods of low-oxygen and elevated temperatures affect organisms physiologically.

Project description:BackgroundConstant hypoxia (CH) and intermittent hypoxia (IH) occur during several pathological conditions such as asthma and obstructive sleep apnea. Our research is focused on understanding the molecular mechanisms that lead to injury or adaptation to hypoxic stress using Drosophila as a model system. Our current genome-wide study is designed to investigate gene expression changes and identify protective mechanism(s) in D. melanogaster after exposure to severe (1% O(2)) intermittent or constant hypoxia.Methodology/principal findingsOur microarray analysis has identified multiple gene families that are up- or down-regulated in response to acute CH or IH. We observed distinct responses to IH and CH in gene expression that varied in the number of genes and type of gene families. We then studied the role of candidate genes (up-or down-regulated) in hypoxia tolerance (adult survival) for longer periods (CH-7 days, IH-10 days) under severe CH or IH. Heat shock proteins up-regulation (specifically Hsp23 and Hsp70) led to a significant increase in adult survival (as compared to controls) of P-element lines during CH. In contrast, during IH treatment the up-regulation of Mdr49 and l(2)08717 genes (P-element lines) provided survival advantage over controls. This suggests that the increased transcript levels following treatment with either paradigm play an important role in tolerance to severe hypoxia. Furthermore, by over-expressing Hsp70 in specific tissues, we found that up-regulation of Hsp70 in heart and brain play critical role in tolerance to CH in flies.Conclusions/significanceWe observed that the gene expression response to IH or CH is specific and paradigm-dependent. We have identified several genes Hsp23, Hsp70, CG1600, l(2)08717 and Mdr49 that play an important role in hypoxia tolerance whether it is in CH or IH. These data provide further clues about the mechanisms by which IH or CH lead to cell injury and morbidity or adaptation and survival.

Project description:Nocturnally active gymnotiform weakly electric fish generate electric signals for communication and navigation, which can be energetically taxing. These fish mainly inhabit the Amazon basin, where some species prefer well-oxygenated waters and others live in oxygen-poor, stagnant habitats. The latter species show morphological, physiological, and behavioral adaptations for hypoxia-tolerance. However, there have been no studies of hypoxia tolerance on the molecular level. Globins are classic respiratory proteins. They function principally in oxygen-binding and -delivery in various tissues and organs. Here, we investigate the molecular evolution of alpha and beta hemoglobins, myoglobin, and neuroglobin in 12 gymnotiforms compared with other teleost fish.The present study identified positively selected sites (PSS) on hemoglobin (Hb) and myoglobin (Mb) genes using different maximum likelihood (ML) methods; some PSS fall in structurally important protein regions. This evidence for the positive selection of globin genes suggests that the adaptive evolution of these genes has helped to enhance the capacity for oxygen storage and transport. Interestingly, a substitution of a Cys at a key site in the obligate air-breathing electric eel (Electrophorus electricus) is predicted to enhance oxygen storage of Mb and contribute to NO delivery during hypoxia. A parallel Cys substitution was also noted in an air-breathing African electric fish (Gymnarchus niloticus). Moreover, the expected pattern under normoxic conditions of high expression of myoglobin in heart and neuroglobin in the brain in two hypoxia-tolerant species suggests that the main effect of selection on these globin genes is on their sequence rather than their basal expression patterns.Results indicate a clear signature of positive selection in the globin genes of most hypoxia-tolerant gymnotiform fishes, which are obligate or facultative air breathers. These findings highlight the critical role of globin genes in hypoxia tolerance evolution of Gymnotiform electric fishes.

Dataset Information

Mechanisms and evolution of hypoxia tolerance in fish.

Publications

Mechanisms and evolution of hypoxia tolerance in fish.

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