Transcriptome and Molecular Pathway Analysis of the Hepatopancreas in the Pacific White Shrimp Litopenaeus vannamei under Chronic Low-Salinity Stress

PLOS ONE, Dec 2019

The Pacific white shrimp Litopenaeus vannamei is a euryhaline penaeid species that shows ontogenetic adaptations to salinity, with its larvae inhabiting oceanic environments and postlarvae and juveniles inhabiting estuaries and lagoons. Ontogenetic adaptations to salinity manifest in L. vannamei through strong hyper-osmoregulatory and hypo-osmoregulatory patterns and an ability to tolerate extremely low salinity levels. To understand this adaptive mechanism to salinity stress, RNA-seq was used to compare the transcriptomic response of L. vannamei to changes in salinity from 30 (control) to 3 practical salinity units (psu) for 8 weeks. In total, 26,034 genes were obtained from the hepatopancreas tissue of L. vannamei using the Illumina HiSeq 2000 system, and 855 genes showed significant changes in expression under salinity stress. Eighteen top Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were significantly involved in physiological responses, particularly in lipid metabolism, including fatty-acid biosynthesis, arachidonic acid metabolism and glycosphingolipid and glycosaminoglycan metabolism. Lipids or fatty acids can reduce osmotic stress in L. vannamei by providing additional energy or changing the membrane structure to allow osmoregulation in relevant organs, such as the gills. Steroid hormone biosynthesis and the phosphonate and phosphinate metabolism pathways were also involved in the adaptation of L. vannamei to low salinity, and the differential expression patterns of 20 randomly selected genes were validated by quantitative real-time PCR (qPCR). This study is the first report on the long-term adaptive transcriptomic response of L. vannamei to low salinity, and the results will further our understanding of the mechanisms underlying osmoregulation in euryhaline crustaceans.

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Transcriptome and Molecular Pathway Analysis of the Hepatopancreas in the Pacific White Shrimp Litopenaeus vannamei under Chronic Low-Salinity Stress

July Transcriptome and Molecular Pathway Analysis of the Hepatopancreas in the Pacific White Shrimp Litopenaeus vannamei under Chronic Low-Salinity Stress Ke Chen 0 1 Erchao Li 0 1 Tongyu Li 0 1 Chang Xu 0 1 Xiaodan Wang 0 1 Heizhao Lin 0 1 Jian G. Qin 0 1 Liqiao Chen 0 1 0 1 Laboratory of Aquaculture Nutrition and Environmental Health, School of Life Sciences, East China Normal University , Shanghai , China , 2 Shenzhen Base of South China Sea Fisheries Research Institute , Shenzhen , China , 3 School of Biological Sciences, Flinders University , Adelaide , Australia 1 Editor: Peng Xu, Chinese Academy of Fishery Sciences , CHINA The Pacific white shrimp Litopenaeus vannamei is a euryhaline penaeid species that shows ontogenetic adaptations to salinity, with its larvae inhabiting oceanic environments and postlarvae and juveniles inhabiting estuaries and lagoons. Ontogenetic adaptations to salinity manifest in L. vannamei through strong hyper-osmoregulatory and hypo-osmoregulatory patterns and an ability to tolerate extremely low salinity levels. To understand this adaptive mechanism to salinity stress, RNA-seq was used to compare the transcriptomic response of L. vannamei to changes in salinity from 30 (control) to 3 practical salinity units (psu) for 8 weeks. In total, 26,034 genes were obtained from the hepatopancreas tissue of L. vannamei using the Illumina HiSeq 2000 system, and 855 genes showed significant changes in expression under salinity stress. Eighteen top Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways were significantly involved in physiological responses, particularly in lipid metabolism, including fatty-acid biosynthesis, arachidonic acid metabolism and glycosphingolipid and glycosaminoglycan metabolism. Lipids or fatty acids can reduce osmotic stress in L. vannamei by providing additional energy or changing the membrane structure to allow osmoregulation in relevant organs, such as the gills. Steroid hormone biosynthesis and the phosphonate and phosphinate metabolism pathways were also involved in the adaptation of L. vannamei to low salinity, and the differential expression patterns of 20 randomly selected genes were validated by quantitative real-time PCR (qPCR). This study is the first report on the long-term adaptive transcriptomic response of L. vannamei to low salinity, and the results will further our understanding of the mechanisms underlying osmoregulation in euryhaline crustaceans. - center (ZF1206), and partly by the E-Institute of Shanghai Municipal Education Commission (No. E03009) and ECNU innovation fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Salinity is one of the main environmental factors that exert a selection pressure on aquatic organisms, and variations in ambient salinity can directly impact the composition and osmolality of body fluids in aquatic animals [1]. Aquatic crustaceans inhabit environments with varying salinities, such as freshwater to seawater, and a change of environment requires crustaceans to regulate hemolymph osmolytes via osmoregulation [2, 3]. Crustaceans display several patterns of osmoregulation, including osmoconformation, hyper-osmoregulation and hypoosmoregulation [2, 4]. Studies have shown that salinity stress can reduce salt diffusion between hemolymph and the environment because water is absorbed from the medium, which leads to swollen cells [5]. When confronted with salinity stress, aquatic animals are forced to osmoregulate by altering the expression of various enzymes and transporters, and the physiological adaptations associated with such functional changes are energy intensive [6]. Therefore, it is important to determine the amount of energy that is required during adaptations to different salinities. In addition, although the biochemical osmoregulation mechanisms of crustaceans have been studied [1, 3, 4], the molecular adaptive mechanisms for energy mobilization are not known. The Pacific white shrimp Litopenaeus vannamei is a typical euryhaline crustacean species that lives in coastal and oceanic environments, and its larvae develop in the ocean, whereas the postlarvae, juveniles and adults live in estuaries and lagoons [7]. A hyper-hypo-osmoregulation process exists in the life history of L. vannamei, and an adaptive mechanism must exist to cope with the environmental salinity fluctuation or long-term low salinity stress. Therefore, L. vannamei can serve as an animal model in the study of adaptive mechanisms in euryhaline crustacean to changes in salinity. Because L. vannamei is an important commercial penaeid species in inland aquaculture at low salinity, extensive research has been conducted on its osmoregulation capabilities. However, inconsistent results have been found in the literature regarding the iso-osmotic point for growth and survival [8–11] (...truncated)


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Ke Chen, Erchao Li, Tongyu Li, Chang Xu, Xiaodan Wang, Heizhao Lin, Jian G. Qin, Liqiao Chen. Transcriptome and Molecular Pathway Analysis of the Hepatopancreas in the Pacific White Shrimp Litopenaeus vannamei under Chronic Low-Salinity Stress, PLOS ONE, 2015, Volume 10, Issue 7, DOI: 10.1371/journal.pone.0131503