Acclimation to prolonged hypoxia alters hemoglobin isoform expression and increases hemoglobin oxygen affinity and aerobic performance in a marine fish

Yihang K Pan,Rasmus Ern,Andrew J Esbaugh,Phillip R Morrison,Colin J Brauner

doi:10.1038/s41598-017-07696-6

Yihang K Pan, Rasmus Ern + Show 3 more

Open Access

https://doi.org/10.1038/s41598-017-07696-6

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Abstract

Hemoglobin (Hb) multiplicity is common in fish, yet despite its ubiquitous nature, the functional significance is unclear. Here we explore the hypothesis that Hb multiplicity plays a role in hypoxia tolerance using the red drum (Sciaenops ocellatus). Red drum is an economically and ecologically important species native to coastal regions and estuaries of the Gulf of Mexico – habitats that routinely experience pronounced hypoxic events. Using a transcriptomic approach, we demonstrate that red drum red blood cells express 7 and 5 Hbα and Hbβ isoforms, respectively. Phylogenetic analysis grouped these isoforms into distinct isoHb clades, and provided evidence of lineage specific expression of particular isoHbs. In normoxia, three isoHbs predominated (Hbα-3.1, -3.2, and Hbβ-3.1). A three-week hypoxia acclimation (48 mmHg) resulted in significant up-regulation of Hbα-2, Hbα-3.2, and Hbβ-3.1, effectively switching the predominantly expressed isoforms. Changes in subunit expression were correlated with a decrease in non-stripped hemolysate P50. Similarly, hypoxia acclimation resulted in a 20% reduction in whole animal critical oxygen threshold (Pcrit). Hypoxia acclimation was not associated with changes in gill morphology, hematocrit, or relative ventricular mass. Overall, these data provide support for the hypothesis that Hb isoform switching can provide a physiological benefit to counteract environmental stress in fishes.

Highlights

Hemoglobin (Hb) multiplicity is a well-documented phenomenon in fish[1,2,3,4,5,6,7]
This species has been shown to exhibit phenotypic plasticity in response to a wide array of environmental perturbations[20,21,22,23]. These factors make red drum an ideal species to explore the capacity of a marine fish to acclimate to prolonged hypoxia through phenotypic plasticity, and whether Hb multiplicity may play a role in this plasticity
The current study sought to explore the ability of red drum – a coastal marine fish native to the Gulf of Mexico – to acclimate to prolonged hypoxia through alterations in blood oxygen transport properties, and the specific role that Hb multiplicity may play in such alterations

Summary

Introduction

Hemoglobin (Hb) multiplicity is a well-documented phenomenon in fish[1,2,3,4,5,6,7]. Hb isoforms (isoHbs) in teleosts are classified into three broad categories[8]. Japanese eel (Anguilla japonica) express at least two functionally distinct Hb pools[7], and acclimation to varying temperatures has been demonstrated to differentially regulate isoHbs in several species[1, 16, 17] These findings suggest that Hb multiplicity may confer www.nature.com/scientificreports/. A second objective sought to explore the effect of prolonged environmental hypoxia on Hb expression, blood oxygen affinity and whole animal critical oxygen thresholds (Pcrit) These studies addressed the potential roles of branchial plasticity in hypoxia acclimation through the analysis of gill surface area and diffusion distance

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