Abstract
The African lungfish, Protopterus annectens, is ammonotelic in water despite being ureogenic. When it aestivates in mucus cocoon on land, ammonia is detoxified to urea. During the maintenance phase of aestivation, urea accumulates in the body, which is subsequently excreted upon arousal. Urea excretion involves urea transporters (UT/Ut). This study aimed to clone and sequence the ut isoforms from the gills of P. annectens, and to test the hypothesis that the mRNA and/or protein expression levels of ut/Ut isoforms could vary in the gills of P. annectens during the induction, maintenance, and arousal phases of aestivation. Two isoforms of ut, ut-a2a and ut-a2b, were obtained from the gills of P. annectens. ut-a2a consisted of 1227 bp and coded for 408 amino acids with an estimated molecular mass of 44.7 kDa, while ut-a2b consisted of 1392 bp and coded for 464 amino acids with an estimated molecular mass of 51.2 kDa. Ut-a2a and Ut-a2b of P. annectens had a closer phylogenetic relationship with Ut/UT of tetrapods than Ut of fishes. While the mRNA expression pattern of ut-a2a and ut-a2b across various tissues of P. annectens differed, the transcript levels of ut-a2a and ut-a2b in the gills were comparable, indicating that they might be equally important for branchial urea excretion during the initial arousal phase of aestivation. During the maintenance phase of aestivation, the transcript level of ut-a2a increased significantly, but the protein abundance of Ut-a2a remained unchanged in the gills of P. annectens. This could be an adaptive feature to prepare for an increase in the production of Ut-a2a upon arousal. Indeed, arousal led to a significant increase in the branchial Ut-a2a protein abundance. Although the transcript level of ut-a2b remained unchanged, there were significant increases in the protein abundance of Ut-a2b in the gills of P. annectens throughout the three phases of aestivation. The increase in the protein abundance of Ut-a2b during the maintenance phase could also be an adaptive feature to prepare for efficient urea excretion when water becomes available.
Highlights
Lungfishes are an archaic group of Sarcopterygian fishes that possess lung for air-breathing
Q24, V25, F27, L84, T130, V188, L247, and T294 of dvUT are conserved in Ut-a2a and Ut-a2b of P. annectens
The replacement of F80, F190, and F243 in dvUT with tyrosine, glycine and tyrosine, respectively, in Ut-a2a and Ut-a2b of P. annectens could potentially alter the shape of urea pore and transport selectivity
Summary
Lungfishes are an archaic group of Sarcopterygian fishes that possess lung for air-breathing. During the induction phase of aestivation, the aestivating lungfish detects cues from the environment and turns them into internal signals that result in behavioral, physiological, structural, and biochemical changes to prepare for the maintenance phase. During the maintenance phase of aestivation, the lungfish is fully encased in a cocoon and all locomotor and feeding activities cease. The lungfish can perpetuate to aestivate in these conditions in the laboratory for more than a year, during which it has to preserve biological structures, avoid cell death, and sustain a slow rate of waste production to prevent pollution of the internal environment. The lungfish can be aroused from aestivation upon the addition of water It has to excrete the accumulated waste products and feed for growth and repair during the arousal phase of aestivation. While metabolic changes are expected to vary between the three phases of aestivation, most reports in the literature focus mainly on the maintenance phase
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