Abstract
Bicarbonate (HCO3–) transport mechanisms play an essential role in the acid-base homeostasis of aquatic animals, and anion exchange protein 3 (AE3) is a membrane transport protein that exchanges Cl–/HCO3– across the cell membrane to regulate the intracellular pH. In this study, the full-length cDNA of AE3 (Lv-AE3) was obtained from the Pacific white shrimp (Litopenaeus vannamei). The Lv-AE3 cDNA is 4,943 bp in length, contains an open reading frame of 2,850 bp, coding for a protein of 949 amino acids with 12 transmembrane domains. Lv-AE3 shows high sequence homology with other AE3 at the protein level. Lv-AE3 mRNA was ubiquitously detected in all tissues selected, with the highest expression level in the gill, followed by the ovary, eyestalk and brain. By in situ hybridization, Lv-AE3-positive cells were shown predominant localization in the secondary gill filaments. The expression levels of Lv-AE3 were further investigated during the essential life processes of shrimp, including ontogeny, molting, and ovarian development. In this case, the spatiotemporal expression profiles of Lv-AE3 in L. vannamei were highly correlated with the activities of water and ion absorption; for example, increased mRNA levels were present after hatching, during embryonic development, after ecdysis during the molt cycle, and in the stage IV ovary during gonadal development. After low/high pH and low/high salinity challenges, the transcript levels of Lv-AE3 were reduced in the gill, while the cell apoptosis rate increased. In addition, knockdown of Lv-AE3 mRNA expression induced cell apoptosis in the gill, indicating a potential link between Lv-AE3 and gill damage. Altogether, this study thoroughly investigated the relationship between the mRNA expression profiles of Lv-AE3 and multiple developmental and physiological processes in L. vannamei, and it may benefit the protection of crustaceans from fluctuated aquatic environments.
Highlights
Global shrimp production is focused on a few species, of which the Pacific white shrimp (Litopenaeus vannamei) is dominant
A partial sequence for L. vannamei AE3 gene was found in a transcriptomic database constructed by our laboratory previously (Li et al, 2020), and the full length cDNA of Lv-AE3 was obtained by 3 - and 5 -rapid amplification of cDNA ends (RACE)
Given that the ovary and hepatopancreas are the key tissues for female shrimp gonadal development and that the gill is the predominant tissue for LvAE3 mRNA expression, the samples were collected from the ovaries, hepatopancreas and gills in four ovarian developmental stages with five individuals, and the Lv-AE3 mRNA levels were analysed by quantitative real-time PCR (qPCR) as described above
Summary
Global shrimp production is focused on a few species, of which the Pacific white shrimp (Litopenaeus vannamei) is dominant. Multiple developmental and physiological processes of crustaceans that are crucial for aquaculture, such as ontogeny, molting (deVries et al, 2016) and gonadal development, may be affected by the water pH. In this case, ion transport is one of the most significant mechanisms for maintaining pH homeostasis in aquatic crustaceans, and it enables crustaceans to cope with pH variations in aquatic water (Chen and Lee, 1997; Cai et al, 2017). The anion exchanger family, related to bicarbonate transport, is a member of the amino acid-polyamineorganocation (APC) superfamily (Vastermark et al, 2014) All members in this family exchange anions across cellular barriers to regulate pH homeostasis. This study provides new understanding of AE3 under multiple developmental and physiological processes and may benefit crustaceans farming in aquatic environments with fluctuating pH and salinity
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