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RNA-seq Provides Novel Insights into Response to Acute Salinity Stress in Oriental River Prawn Macrobrachium nipponense

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Abstract

The oriental river prawn Macrobrachium nipponense is an important aquaculture species in China, Vietnam, and Japan. This species could survive in the salinity ranging from 7 to 20 ppt and accelerate growth in the salinity of 7 ppt. To identify the genes and pathways in response to acute high salinity stress, M. nipponense was exposed to the acute high salinity of 25 ppt. Total RNA from hepatopancreas, gills, and muscle tissues was isolated and then sequenced using high-throughput sequencing method. Differentially expressed genes (DGEs) were identified, and a total of 632, 836, and 1246 DEGs with a cutoff of significant twofold change were differentially expressed in the hepatopancreas, gills, and muscle tissues, respectively. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genome pathway enrichment analyses were conducted. These DEGs were involved in the GO terms of cellular process, metabolic process, membrane, organelle, binding, and catalytic activity. The DEGs of hepatopancreas and gill tissues were mainly enriched in PPAR signaling pathway, longevity regulating pathway, protein digestion and absorption, and the DEGs of muscle tissue in arginine biosynthesis, adrenergic signaling in cardiomyocytes, cardiac muscle contraction, and cGMP-PKG signaling pathway. Real-time PCR conducted with fifteen selected DEGs indicated high reliability of digital analysis using RNA-Seq. The results indicated that the M. nipponense may regulate essential mechanisms such as metabolism, oxidative stress, and ion exchange to adapt the alternation of environment, when exposed to acute high salinity stress. This work reveals the numbers of genes modified by salinity stress and some important pathways, which could provide a comprehensive insight into the molecular responses to high salinity stress in M. nipponense and further boost the understanding of the potential molecular mechanisms of adaptation to salinity stress for euryhaline crustaceans.

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References

  • Aguilar C, Raina JB, Fôret S et al (2019) Transcriptomic analysis reveals protein homeostasis breakdown in the coral Acropora millepora during hypo-saline stress. BMC Genomics 20:1–14

  • Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level–the DESeq package. DESq Man 1–28

  • Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    Article  CAS  Google Scholar 

  • Aranguren Caro LF, Alghamdi F, De Belder K et al (2021) The effect of salinity on Enterocytozoon hepatopenaei infection in Penaeus vannamei under experimental conditions. BMC Vet Res 17:1–9

    Article  Google Scholar 

  • Aranyakanont C, Ijiri S, Hasegawa Y, Adachi S (2020) 17β-Hydroxysteroid dehydrogenase type 12 is responsible for maturation-inducing steroid synthesis during oocyte maturation in Nile tilapia. Gen Comp Endocrinol 290

  • Bertucci JI, Tovar MO, Blanco AM et al (2017) Influence of water salinity on genes implicated in somatic growth, lipid metabolism and food intake in pejerrey (Odontesthes bonariensis). Comp Biochem Physiol Part B Biochem Mol Biol 210:29–38

  • Bolger A, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data Bioinformatics 30. https://doi.org/10.1093/bioinformatics/btu170

  • Carmosino M, Rizzo F, Torretta S et al (2013) High-throughput fluorescent-based NKCC functional assay in adherent epithelial cells. BMC Cell Biol 14:1. https://doi.org/10.1186/1471-2121-14-16

    Article  CAS  Google Scholar 

  • Chan QWT Melathopoulos AP, Pernal SF, Foster LJ (2009) The innate immune and systemic response in honey bees to a bacterial pathogen Paenibacillus Larvae BMC Genomics 10. https://doi.org/10.1186/1471-2164-10-387

  • Chen K, Li E-C, Gan L et al (2014) Growth and lipid metabolism of the Pacific white shrimp Litopenaeus vannamei at different salinities J Shellfish Res 33. https://doi.org/10.2983/035.033.0317

  • Chen K, Li E, Li T et al (2015) Transcriptome and molecular pathway analysis of the hepatopancreas in the Pacific white shrimp Litopenaeus vannamei under chronic low-salinity stress. PLoS One 10:1–22

    Google Scholar 

  • Chen Q, Zhang Y, Zhao Q (2020) Expression analysis of immune-associated genes in hemocytes of mud crab Scylla paramamosain under low salinity challenge. Fish Shellfish Immunol 107:16–25

    Article  CAS  Google Scholar 

  • Chourasia TK (2018) Effects of the acclimation to high salinity on intestinal ion and peptide transporters in two tilapia species that differ in their salinity tolerance. Comp Biochem Physiol Part A Mol Integr Physiol

  • Chung K-F, Lin H-C (2006) Osmoregulation and Na, K-ATPase expression in osmoregulatory organs of Scylla paramamosain. Comp Biochem Physiol Part A Mol Integr Physiol 144:48–57

  • Dahout-Gonzalez C, Nury H, Trézéguet V et al (2006) Molecular, functional, and pathological aspects of the mitochondrial ADP/ATP carrier. Physiology (bethesda) 21:242–249

    CAS  Google Scholar 

  • Deane EE, Woo NYS (2004) Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). Am J Physiol Regul Integr Comp Physiol 287:R1054–R1063

    Article  CAS  Google Scholar 

  • Ding Z, Zhou J, Kong Y et al (2017) Dietary arachidonic acid promotes growth, improves immunity, and regulates the expression of immune-related signaling molecules in Macrobrachium nipponense (De Haan) Aquaculture 484. https://doi.org/10.1016/j.aquaculture.2017.11.010

  • Do H, Yang W, Okuno A, Wilder M (2001) Changes in free amino acids in the hemolymph of giant freshwater prawn Macrobrachium rosenbergii exposed to varying salinities: Relationship to osmoregulatory ability. Comp Biochem Physiol A Mol Integr Physiol 128:317–326

    Article  Google Scholar 

  • Giménez L, Anger K (2001) Relationships among salinity, egg size, embryonic development, and larval biomass in the estuarine crab Chasmagnathus granulata Dana, 1851. J Exp Mar Bio Ecol 260:241–257

    Article  Google Scholar 

  • Hiltunen JK, Kastaniotis AJ, Autio KJ et al (2019) 17B-Hydroxysteroid dehydrogenases as acyl thioester metabolizing enzymes. Mol Cell Endocrinol 489:107–118

    Article  CAS  Google Scholar 

  • Hiroi J, Yasumasu S, McCormick SD et al (2008) Evidence for an apical Na-Cl cotransporter involved in ion uptake in a teleost fish. J Exp Biol 211:2584–2599

    Article  CAS  Google Scholar 

  • Huang Y, Zhang M, Li Y et al (2019) Effects of salinity acclimation on the growth performance, osmoregulation and energy metabolism of the oriental river prawn, Macrobrachium nipponense (De Haan). Aquac Res 50:685–693

    Article  CAS  Google Scholar 

  • Jin S, Bian C, Jiang S et al (2021) A chromosome-level genome assembly of the oriental river prawn, Macrobrachium nipponense. Gigascience 10:1–9

    Article  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S et al (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  Google Scholar 

  • Khodabandeh S, Guy C, Charmantier-Daures M (2005) Ultrastructural studies and Na+, K+-ATPase immunolocalization in the antennal urinary glands of the lobster Homarus gammarus (Crustacea, Decapoda). J Histochem Cytochem 53:1203–1214

    Article  CAS  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  Google Scholar 

  • Kregel KC (2002) Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92:2177–2186

    Article  CAS  Google Scholar 

  • Li E, Wang S, Li C et al (2014) Transcriptome sequencing revealed the genes and pathways involved in salinity stress of Chinese mitten crab, Eriocheir sinensis. Physiol Genomics 46:177–190

    Article  CAS  Google Scholar 

  • Li F, Xiang J (2013) Recent advances in researches on the innate immunity of shrimp in China. Dev Comp Immunol 39:11–26

  • Lindqvist O V (2004) Crustacean farming: ranching and culture: John F. Wickins and Daniel O’C. Lee. 2nd Edition. Blackwell Science, Oxford, UK. 2002. 446 pp., price GBP 85, ISBN 0 632 05464 6. Aquaculture 235:659–660

  • Liu S, Wang X, Sun F et al (2013) RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish. Physiol Genomics 45:462–476. https://doi.org/10.1152/physiolgenomics.00026.2013

    Article  CAS  PubMed  Google Scholar 

  • Lou F, Gao T, Han Z (2019) Effect of salinity fluctuation on the transcriptome of the Japanese mantis shrimp Oratosquilla oratoria Int J Biol Macromol 140. https://doi.org/10.1016/j.ijbiomac.2019.08.223

  • Luu-The V, Tremblay P, Labrie F (2006) Characterization of type 12 17beta-hydroxysteroid dehydrogenase, an isoform of type 3 17beta-hydroxysteroid dehydrogenase responsible for estradiol formation in women. Mol Endocrinol 20:437–443

    Article  CAS  Google Scholar 

  • Ma K, Qiu G, Feng J, Li J (2012) Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS One 7

  • Mathew S, Ashok Kumar K, Anandan R, et al (2007) Changes in tissue defence system in white spot syndrome virus (WSSV) infected Penaeus monodon. Comp Biochem Physiol Part C Toxicol Pharmacol 145:315–320

  • Nikapitiya C, Kim W-S, Park K, Kwak I-S (2014) Identification of potential markers and sensitive tissues for low or high salinity stress in an intertidal mud crab (Macrophthalmus japonicus). Fish Shellfish Immunol 41:407–416

  • Palacios E, Racotta IS (2007) Salinity stress test and its relation to future performance and different physiological responses in shrimp postlarvae. Aquaculture 268:123–135

    Article  CAS  Google Scholar 

  • Pan L-Q, Zhang L-J, Liu H-Y (2007) Effects of salinity and pH on ion-transport enzyme activities, survival and growth of Litopenaeus vannamei postlarvae. Aquaculture 273:711–720

  • Pan L, Liu H, Zhao Q (2014) Effect of salinity on the biosynthesis of amines in Litopenaeus vannamei and the expression of gill related ion transporter genes. J Ocean Univ China 13:453–459

  • Roberts A, Trapnell C, Donaghey J et al (2011) Improving RNA-seq expression estimates by correcting for fragment bias. Genome Biol 12(3):R22. Genome Biol 12:R22

  • Romano N, Zeng C (2011) Importance of balanced Na+/K+ ratios for blue swimmer crabs, Portunus pelagicus, to cope with elevated ammonia-N and differences between in vitro and in vivo gill Na+/K+-ATPase responses. Aquaculture 318:154–161

  • Sui L, Wille M, Cheng Y, Sorgeloos P (2007) The effect of dietary n-3 HUFA levels and DHA/EPA ratios on growth, survival and osmotic stress tolerance of Chinese mitten crab Eriocheir sinensis larvae. Aquaculture 273:139–150

  • Sun S, Xuan F, Fu H et al (2015) Transciptomic and histological analysis of hepatopancreas, muscle and gill tissues of oriental river prawn (Macrobrachium nipponense) in response to chronic hypoxia. BMC Genomics 16:1–13

  • Tang T, Ji C, Yang Z et al (2017) Involvement of the Macrobrachium nipponense rhodanese homologue 2, MnRDH2 in innate immunity and antioxidant defense. Fish Shellfish Immunol 70:327–334

  • Tantulo U, Fotedar R (2006) Comparison of growth, osmoregulatory capacity, ionic regulation and organosomatic indices of black tiger prawn (Penaeus monodon Fabricius, 1798) juveniles reared in potassium fortified inland saline water and ocean water at different salinities. Aquaculture 258:594–605

  • Trapnell C, Williams BA, Pertea G et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

  • Velotta JP, McCormick SD, O’Neill RJ, Schultz ET (2014) Relaxed selection causes microevolution of seawater osmoregulation and gene expression in landlocked Alewives. Oecologia 175:1081–1092

  • Wang H, Tang L, Wei H et al (2018) Transcriptomic analysis of adaptive mechanisms in response to sudden salinity drop in the mud crab, Scylla paramamosain. BMC Genomics 19:1–12

  • Wang W, Sun R, Wang A et al (2002) Effect of different environmental factors on the activities of digestive enzymes and alkaline phosphatase of Macrobrachium nipponense. Ying Yong Sheng Tai Xue Bao 13:1153–1156

    CAS  PubMed  Google Scholar 

  • Wang Y, Li Z, Li J et al (2015) Effects of dietary chlorogenic acid on growth performance, antioxidant capacity of white shrimp Litopenaeus vannamei under normal condition and combined stress of low-salinity and nitrite. Fish Shellfish Immunol 43:337–345

  • Wheatly MG, Zanotto FP, Hubbard MG (2002) Calcium homeostasis in crustaceans: subcellular Ca dynamics. Comp Biochem Physiol Part B Biochem Mol Biol 132:163–178

  • Ying W (2007) NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10:179–206

  • Yu J, Sun J, Zhao S et al (2019) Transcriptome analysis of oriental river Prawn(Macrobrachium nipponense) hepatopancreas in response to ammonia exposure. Fish Shellfish Immunol 93:223–231

  • Zhang Y, Jiang S, Qiao H et al (2021) Transcriptome analysis of five ovarian stages reveals gonad maturation in female Macrobrachium nipponense. BMC Genomics 22:1–12.

    Article  CAS  Google Scholar 

  • Zheng X, Duan Y, Dong H, Zhang J (2017) Effects of dietary Lactobacillus plantarum in different treatments on growth performance and immune gene expression of white shrimp Litopenaeus vannamei under normal condition and stress of acute low salinity. Fish Shellfish Immunol 62:195–201

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Innovation Action Plan project of the Science and Technology Commission of Shanghai Municipality (19391900900, 21002410500), Guangdong Provincial Key R&D Program.

(2020B0202010001), and Special Fund for Science and Technology Development of Shanghai Ocean University.

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Authors and Affiliations

  1. Key Laboratory of Freshwater Aquatic Genetic Resources Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai, China

    Yaoran Fan, Jianbin Feng, Feiyue Ling, Zefei Wang, Keyi Ma, Xueming Hua & Jiale Li

  2. National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, China

    Yaoran Fan, Jianbin Feng, Feiyue Ling, Zefei Wang, Keyi Ma, Xueming Hua & Jiale Li

  3. Shanghai Engineering Research Centre of Aquaculture, Shanghai Ocean University, Shanghai, China

    Yaoran Fan, Jianbin Feng, Feiyue Ling, Zefei Wang, Keyi Ma, Xueming Hua & Jiale Li

  4. Hangzhou Fishery Research Institute, Hangzhou, China

    Nan Xie

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  1. Yaoran Fan
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Contributions

Jianbin Feng and Jiale Li conceptualized the study. Yaoran Fan, Feiyue Ling, Zefei Wang, and Xie Nan collected the specimens and experimented. Yaoran Fan performed the qRT-PCR and bioinformatics work. Yaoran Fan and Jianbin Feng participated in the formal analysis of the results. Yaoran Fan drafted the manuscript. Jianbin Feng, Xueming Hua, and Keyi Ma critically evaluated and approved the article.

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Correspondence to Jiale Li.

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Yaoran Fan and Jianbin Feng contributed equally to this study.

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Fan, Y., Feng, J., Xie, N. et al. RNA-seq Provides Novel Insights into Response to Acute Salinity Stress in Oriental River Prawn Macrobrachium nipponense. Mar Biotechnol 24, 820–829 (2022). https://doi.org/10.1007/s10126-022-10151-x

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