Characteristic Metabolism of Free Amino Acids in Cetacean Plasma: Cluster Analysis and Comparison with Mice

Kazuki Miyaji,Dai Ohtsu,Fumio Terasawa,Makoto Bannai,Kenji Nagao,Shu Ito,Kaoru Kohyama,Mitsuaki Ohta,Hajime Iwao,Nobuyo Ohtani,Hiroshi Asakawa

doi:10.1371/journal.pone.0013808

Kazuki Miyaji, Dai Ohtsu + Show 9 more

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https://doi.org/10.1371/journal.pone.0013808

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Abstract

From an evolutionary perspective, the ancestors of cetaceans first lived in terrestrial environments prior to adapting to aquatic environments. Whereas anatomical and morphological adaptations to aquatic environments have been well studied, few studies have focused on physiological changes. We focused on plasma amino acid concentrations (aminograms) since they show distinct patterns under various physiological conditions. Plasma and urine aminograms were obtained from bottlenose dolphins, pacific white-sided dolphins, Risso's dolphins, false-killer whales and C57BL/6J and ICR mice. Hierarchical cluster analyses were employed to uncover a multitude of amino acid relationships among different species, which can help us understand the complex interrelations comprising metabolic adaptations. The cetacean aminograms formed a cluster that was markedly distinguishable from the mouse cluster, indicating that cetaceans and terrestrial mammals have quite different metabolic machinery for amino acids. Levels of carnosine and 3-methylhistidine, both of which are antioxidants, were substantially higher in cetaceans. Urea was markedly elevated in cetaceans, whereas the level of urea cycle-related amino acids was lower. Because diving mammals must cope with high rates of reactive oxygen species generation due to alterations in apnea/reoxygenation and ischemia-reperfusion processes, high concentrations of antioxidative amino acids are advantageous. Moreover, shifting the set point of urea cycle may be an adaption used for body water conservation in the hyperosmotic sea water environment, because urea functions as a major blood osmolyte. Furthermore, since dolphins are kept in many aquariums for observation, the evaluation of these aminograms may provide useful diagnostic indices for the assessment of cetacean health in artificial environments in the future.

Highlights

From an evolutionary perspective, the ancestors of cetaceans first lived in a terrestrial environment prior to adapting to an aquatic environment
Since the dendrogram chooses clustering steps that minimize the increase in the error sum of squares at each level, the formation of distinguishable clusters that differ between cetaceans and mice illustrates that the aminogram patterns differ remarkably between these two groups
Since the aim of this study was to unveil the characteristic amino acid metabolism observed in cetaceans, compared with representative terrestrial animals, we chose mice as one of the most intensively investigated terrestrial model animals

Summary

Introduction

The ancestors of cetaceans first lived in a terrestrial environment prior to adapting to an aquatic environment. Certain adaptive physiological properties, such as a higher basal metabolic rate and a lower maximum rate of oxygen consumption [3,4], are illustrated in cetaceans. Diving mammals must cope with higher rates of ROS generation relative to terrestrial mammals due to alterations in apnea/reoxygenation and ischemia-reperfusion processes [5]. Several physiological adaptations for water conservation in cetaceans have been identified, including reduced rate of respiratory water loss [10], the absence of sweat glands [11] and the production of concentrated urine [9], few studies have examined metabolic adaptations to the hyperosmotic environment

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