Skip to main content
SpringerLink
Log in

Comparative Transcriptome Analysis Reveals the Light Spectra Affect the Growth and Molting of Scylla paramamosain by Changing the Chitin Metabolism

  • Research
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Light is an essential ecological factor that has been demonstrated to affect aquatic animals’ behavior, growth performance, and energy metabolism. Our previous study found that the full-spectrum light and cyan light could promote growth performance and molting frequency of Scylla paramamosain while it was suppressed by violet light. Hence, the purpose of this study is to investigate the underlying molecular mechanism that influences light spectral composition on the growth performance and molting of S. paramamosain. RNA-seq analysis and qPCR were employed to assess the differentially expressed genes (DEGs) of eyestalks from S. paramamosain reared under full-spectrum light (FL), violet light (VL), and cyan light (CL) conditions after 8 weeks trial. The results showed that there are 5024 DEGs in FL vs. VL, 3398 DEGs in FL vs. CL, and 3559 DEGs in VL vs. CL observed. GO analysis showed that the DEGs enriched in the molecular function category involved in chitin binding, structural molecular activity, and structural constituent of cuticle. In addition, the DEGs in FL vs. VL were mainly enriched in the ribosome, amino sugar and nucleotide sugar metabolism, lysosome, apoptosis, and antigen processing and presentation pathways by KEGG pathway analysis. Similarly, ribosome, lysosome, and antigen processing and presentation pathways were major terms that enriched in FL vs. CL group. However, only the ribosome pathway was significantly enriched in up-regulated DEGs in VL vs. CL group. Furthermore, five genes were randomly selected from DEGs for qPCR analysis to validate the RNA-seq data, and the result showed that there was high consistency between the RNA-seq and qPCR. Taken together, violet light exposure may affect the growth performance of S. paramamosain by reducing the ability of immunity and protein biosynthesis, and chitin metabolism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Availability of Data and Material

Data will be made available on request. RNA sequencing raw reads have been deposited in NCBI’s Sequence Read Archive (SRA) under BioProject accession number PRJNA897016.

References

  • Abdullah-Zawawi M-R, Afiqah-Aleng N, Ikhwanuddin M, Sung YY, Tola S, Fazhan H, Waiho K (2021) Recent development in ecdysone receptor of crustaceans: current knowledge and future applications in crustacean aquaculture. Rev Aquac 13:1938–1957

    Article  Google Scholar 

  • Amin-Safwan A, Muhd-Farouk H, Mardhiyyah MP, Nadirah M, Ikhwanuddin M (2019) Does water salinity affect the level of 17β-estradiol and ovarian physiology of orange mud crab, Scylla olivacea (Herbst, 1796) in captivity? Journal of King Saud University - Science 31:827–835

    Article  Google Scholar 

  • Barranger A, Langan LM, Sharma V, Rance GA, Aminot Y, Weston NJ, Akcha F, Moore MN, Arlt VM, Khlobystov AN, Readman JW, Jha AN (2019) Antagonistic interactions between benzo[a]pyrene and fullerene (c60) in toxicological response of marine mussels. Nanomaterials 9:987. https://doi.org/10.3390/nano9070987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodsky FM (1992) Antigen processing and presentation: close encounters in the endocytic pathway. Trends Cell Biol 2:109–115

    Article  CAS  PubMed  Google Scholar 

  • Chaharbakhshi E, Jemc JC (2016) Broad-complex, tramtrack, and bric-à-brac (BTB) proteins: critical regulators of development. Genesis 54:505–518

    Article  CAS  PubMed  Google Scholar 

  • Chandhini S, Rejish Kumar VJ (2019) Transcriptomics in aquaculture: current status and applications. Rev Aquac 11:1379–1397

    Article  Google Scholar 

  • Chang ES, Mykles DL (2011) Regulation of crustacean molting: a review and our perspectives. Gen Comp Endocrinol 172:323–330

    Article  CAS  PubMed  Google Scholar 

  • Chang ES, Bruce MJ, Tamone SL (2015) Regulation of crustacean molting: a multi-hormonal system. Am Zool 33:324–329

    Article  Google Scholar 

  • Chen S, Migaud H, Shi C, Song C, Wang C, Ye Y, Ren Z, Wang H, Mu C (2021) Light intensity impacts on growth, molting and oxidative stress of juvenile mud crab Scylla paramamosain. Aquaculture 545:737159

    Article  CAS  Google Scholar 

  • Chen S, Shi C, Migaud H, Song C, Mu C, Ye Y, Wang C, Ren Z (2022) Light spectrum impacts on growth, molting, and oxidative stress response of the mud crab Scylla paramamosain. Front Mar Sci 9:840353

    Article  Google Scholar 

  • Chen S, Liu J, Shi C, Migaud H, Ye Y, Song C, Mu C, Ren Z, Wang C (2023) Effect of photoperiod on growth, survival, and lipid metabolism of mud crab Scylla paramamosain juveniles. Aquaculture 567:739279

    Article  Google Scholar 

  • De Kleijn DPV, Van Herp F (1995) Molecular biology of neurohormone precursors in the eyestalk of Crustacea. Biochem Physiol Part B Biochem Mol Biol 112:573–579

    Article  Google Scholar 

  • Devaraj H, Natarajan A (2006) Molecular mechanisms regulating molting in a crustacean. FEBS J 273:839–846

    Article  CAS  PubMed  Google Scholar 

  • Fanjul-Moles ML (2006) Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update. Comp Biochem Physiol C 142:390–400

    Google Scholar 

  • Fei F, Gao X, Wang X, Liu Y, Bin H, Liu B (2020a) Effect of spectral composition on growth, oxidative stress responses, and apoptosis-related gene expression of the shrimp. Penaeus Vannamei Aquaculture Reports 16:100267

    Article  Google Scholar 

  • Fei F, Liu B, Gao X, Wang X, Liu Y, Bin H (2020b) Effects of supplemental ultraviolet light on growth, oxidative stress responses, and apoptosis-related gene expression of the shrimp Litopenaeus vannamei. Aquaculture 520:735013

    Article  CAS  Google Scholar 

  • Gao X, Zhang M, Li X, Shi C, Song C, Liu Y (2016a) Effects of LED light quality on the growth, metabolism, and energy budgets of Haliotis discus discus. Aquaculture 453:31–39

    Article  CAS  Google Scholar 

  • Gao X, Zhang M, Tian H, Zheng J, Li X, Song C, Liu Y (2016b) Effect of LED light quality on respiratory metabolism and activities of related enzymes of Haliotis discus hannai. Aquaculture 452:52–61

    Article  CAS  Google Scholar 

  • Glantz RM, Kirk MD, Are´Chiga, H. (1983) Light input to crustacean neurosecretory cells. Brain Res 265:307–311

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat Biotechnol 29:644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo B, Wang F, Dong S, Gao Q (2011) The effect of rhythmic light color fluctuation on the molting and growth of Litopenaeus vannamei. Aquaculture 314:210–214

    Article  Google Scholar 

  • Gust KA, Kennedy AJ, Laird JG, Wilbanks MS, Barker ND, Guan X, Melby NL, Burgoon LD, Kjelland ME, Swannack TM (2019) Different as night and day: behavioural and life history responses to varied photoperiods in Daphnia magna. Mol Ecol 28:4422–4438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hao M, Lin Z, Rong H, Zhu D, Wen X (2018) Sterol regulatory element binding protein-1: molecular cloning, tissue distribution and gene expression level in response to nutritional regulation in mud crab, Scylla paramamosain. Biochem Bioph Res Co 505:705–711

    Article  CAS  Google Scholar 

  • Hou C, Song S, Zhu L, Shi L, Tan B, Zhang S (2021) Growth, immunity, and transcriptome response to dietary Wnt/β-catenin pathway activator TWS119 in Penaeus vannamei. Front Mar Sci 8:486

    Article  Google Scholar 

  • Jaishy B, Abel ED (2016) Lipids, lysosomes, and autophagy. J Lipid Res 57:1619–1635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karakatsouli N, Papoutsoglou ES, Sotiropoulos N, Mourtikas D, Stigen-Martinsen T, Papoutsoglou SE (2010) Effects of light spectrum, rearing density and light intensity on growth performance of scaled and mirror common carp Cyprinus carpio reared under recirculating system conditions. Aquacult Eng 42:121–127

    Article  Google Scholar 

  • Krueger F (2012) Trim Galore: a wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Bisufite-Seq) libraries). http://www.bioinformatics.babraham.ac.uk/projects/trim.galore/. Accessed 28 Mar 2016

  • Li J, Sun J, Dong X, Geng X, Qiu G (2019a) Transcriptomic analysis of gills provides insights into the molecular basis of molting in Chinese mitten crab (Eriocheir sinensis). PeerJ 7:e7182

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Y, Han Z, She Q, Zhao Y, Wei H, Dong J, Xu W, Li X, Liang S (2019b) Comparative transcriptome analysis provides insights into the molecular basis of circadian cycle regulation in Eriocheir sinensis. Gene 694:42–49

    Article  CAS  PubMed  Google Scholar 

  • Li N, Zhou J, Wang H, Mu C, Shi C, Liu L, Wang C (2020) Transcriptome analysis of genes and pathways associated with metabolism in Scylla paramamosain under different light intensities during indoor overwintering. BMC Genomics 21:775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Zhao W, Qin C, Yu G, Ma Z, Guo Y, Pan W, Fu Z, Huang X, Chen J (2021) Comparative transcriptome analysis reveals changes in gene expression in sea cucumber (Holothuria leucospilota) in response to acute temperature stress. Comp Biochem Phys D 40:100883

    CAS  Google Scholar 

  • Liu J, Shi C, Ye Y, Ma Z, Mu C, Ren Z, Wu Q, Wang C (2022) Effects of temperature on growth, molting, feed intake, and energy metabolism of individually cultured juvenile mud crab Scylla paramamosain in the recirculating aquaculture system. Water 14(19):2988. https://doi.org/10.3390/w14192988

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206:4393–4412

    Article  CAS  PubMed  Google Scholar 

  • Molcan L (2019) Time distributed data analysis by Cosinor. Online application. BioRxiv: 805960

  • Nasr, M.a.F., Mohammed, H., Hassan, R.A., Swelum, A.A. & Saadeldin, I.M. (2019) Does light intensity affect the behavior, welfare, performance, meat quality, amino acid profile, and egg quality of Japanese quails? Poult Sci 98:3093–3102

    Article  Google Scholar 

  • Nikapitiya C, Kim W-S, Park K, Kim J, Lee M-O, Kwak I-S (2015) Chitinase gene responses and tissue sensitivity in an intertidal mud crab (Macrophthalmus japonicus) following low or high salinity stress. Cell Stress Chaperones 20:517–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’brien, J.J., Kumari, S.S. & Skinner, D.M. (1991) Proteins of crustacean exoskeletons: I. Similarities and differences among proteins of the four exoskeletal layers of four brachyurans. Biol Bull 181:427–441

    Article  PubMed  Google Scholar 

  • Rocha J, Garcia-Carreño FL, Muhlia-Almazán A, Peregrino-Uriarte AB, Yépiz-Plascencia G, Córdova-Murueta JH (2012) Cuticular chitin synthase and chitinase mRNA of whiteleg shrimp Litopenaeus vannamei during the molting cycle. Aquaculture 330:111–115

    Article  Google Scholar 

  • Ruscoe IM, Shelley CC, Williams GR (2004) The combined effects of temperature and salinity on growth and survival of juvenile mud crabs (Scylla serrata Forskål). Aquaculture 238:239–247

    Article  Google Scholar 

  • Santos CA, Andrade SC, Teixeira AK, Farias F, Guerrelhas AC, Rocha JL, Freitas PD (2021) Transcriptome differential expression analysis reveals the activated genes in Litopenaeus vannamei shrimp families of superior growth performance. Aquaculture 531:735871

    Article  CAS  Google Scholar 

  • Shi L, Qiu L, Jiang Z, Xie Z, Dong M, Zhan Z (2023) The influences of green light on locomotion, growth and reproduction in the brown planthopper Nilaparvata lugens. Pest Manag Sci 79:4100–4112. https://doi.org/10.1002/ps.7612

    Article  CAS  PubMed  Google Scholar 

  • Simons A (2010) Fastqc: a quality control tool for high throughput sequence data

  • Stevens C, Croft D, Paull G, Tyler C (2017) Stress and welfare in ornamental fishes: what can be learned from aquaculture? J Fish Biol 91:409–428

    Article  CAS  PubMed  Google Scholar 

  • Synowiecki J, Al-Khateeb NA (2003) Production, properties, and some new applications of chitin and its derivatives. Crit Rev Food Sci Nutr 43:145–171

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Kasagi S, Murakami N, Furufuji S, Kikuchi S, Mizusawa K, Andoh T (2018) Effects of different green light intensities on the growth performance and endocrine properties of barfin flounder Verasper moseri. Gen Comp Endocr 257:203–210

    Article  CAS  PubMed  Google Scholar 

  • Tan SH, Degnan BM, Lehnert SA (2000) The Penaeus monodon chitinase 1 gene is differentially expressed in the hepatopancreas during the molt cycle. Mar Biotechnol 2:126–135

    Article  CAS  Google Scholar 

  • Tharanathan RN, Kittur FS (2003) Chitin—the undisputed biomolecule of great potential. Crit Rev Food Sci Nutr 43:61–87

    Article  CAS  PubMed  Google Scholar 

  • Villamizar N, García-Alcazar A, Sánchez-Vázquez FJ (2009) Effect of light spectrum and photoperiod on the growth, development and survival of European sea bass (Dicentrarchus labrax) larvae. Aquaculture 292:80–86

    Article  Google Scholar 

  • Villamizar N, Blanco-Vives B, Migaud H, Davie A, Carboni S, Sánchez-Vázquez FJ (2011) Effects of light during early larval development of some aquacultured teleosts: a review. Aquaculture 315:86–94

    Article  Google Scholar 

  • Volpato GL, Barreto R (2001) Environmental blue light prevents stress in the fish Nile tilapia. Braz J Med Biol Res 34:1041–1045

    Article  CAS  PubMed  Google Scholar 

  • Wanlem S, Supamattaya K, Tantikitti C, Prasertsan P, Graidist P (2011) Expression and applications of recombinant crustacean hyperglycemic hormone from eyestalks of white shrimp (Litopenaeus vannamei) against bacterial infection. Fish Shellfish Immun 30:877–885

    Article  CAS  Google Scholar 

  • Webster SG (1998) Neuropeptides inhibiting growth and reproduction in crustaceans. Seminar Series-Society for Experimental Biology. Cambridge University Press, Cambridge 1998:33–52

    Google Scholar 

  • Wu W, Lin X, Wang C, Ke J, Wang L, Liu H (2019) Transcriptome of white shrimp Litopenaeus vannamei induced with rapamycin reveals the role of autophagy in shrimp immunity. Fish Shellfish Immun 86:1009–1018

    Article  CAS  Google Scholar 

  • Wu L, Wang Y, Han M, Song Z, Song C, Xu S, Li J, Wang Y, Li X, Yue X (2020) Growth, stress and non-specific immune responses of turbot (Scophthalmus maximus) larvae exposed to different light spectra. Aquaculture 520:734950

    Article  CAS  Google Scholar 

  • Wu L, Wang Y, Li J, Song Z, Xu S, Song C, Han M, Zhao H, Zhou L, Wang Y, Li X, Yue X (2021) Influence of light spectra on the performance of juvenile turbot (Scophthalmus maximus). Aquaculture 533:736191

    Article  CAS  Google Scholar 

  • Yang M, Chen Z, Hu F, Sun J, Ding J, Chang Y, Zhao C (2020) Light spectra regulated foraging and feeding behaviors shed light on stock enhancement of the sea urchin Strongylocentrotus intermedius. Aquaculture Reports 18:100480

    Article  Google Scholar 

  • Yin F, Gao Q, Tang B, Sun P, Han K, Huang W (2016) Transcriptome and analysis on the complement and coagulation cascades pathway of large yellow croaker (Larimichthys crocea) to ciliate ectoparasite Cryptocaryon irritans infection. Fish Shellfish Immun 50:127–141

    Article  CAS  Google Scholar 

  • Zarubin TP, Chang ES, Mykles DL (2009) Expression of recombinant eyestalk crustacean hyperglycemic hormone from the tropical land crab, Gecarcinus lateralis, that inhibits Y-organ ecdysteroidogenesis in vitro. Mol Biol Rep 36:1231–1237

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Yuan J, Sun Y, Li S, Gao Y, Yu Y, Liu C, Wang Q, Lv X, Zhang X, Ma KY, Wang X, Lin W, Wang L, Zhu X, Zhang C, Zhang J, Jin S, Yu K, Kong J, Xu P, Chen J, Zhang H, Sorgeloos P, Sagi A, Alcivar-Warren A, Liu Z, Wang L, Ruan J, Chu KH, Liu B, Li F, Xiang J (2019) Penaeid shrimp genome provides insights into benthic adaptation and frequent molting. Nat Commun 10:356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Yuan J, Li F, Xiang J (2021) Chitin synthesis and degradation in crustaceans: a genomic view and application. Mar Drugs 19:153

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou ZK, Gu WB, Wang C, Zhou YL, Tu DD, Liu ZP, Zhu QH, Shu MA (2018) Seven transcripts from the chitinase gene family of the mud crab Scylla paramamosain: their expression profiles during development and moulting and under environmental stresses. Aquac Res 49:3296–3308

    Article  CAS  Google Scholar 

Download references

Funding

The work was supported by the National Natural Science Foundation of China (Grant Nos. 32172994 and 31972783), the International Cooperation Project of Ningbo City (2023H012), the Province Key Research and Development Program of Zhejiang (2021C02047), Key Scientific and Technological Grant of Zhejiang for Breeding New Agricultural Varieties (2021C02069-6), Collaborative Promotion Program of Zhejiang Provincial Agricultural Technology of China (No. 2020XTTGSC03), SanNongLiuFang Zhejiang Agricultural Science and Technology Cooperation Project (2021SNLF029), 2025 Technological Innovation for Ningbo (No. 2019B10010), China Agriculture Research System of MOF and MARA (No. CARS48), the Special research funding from the Marine Biotechnology and Marine Engineering Discipline Group in Ningbo University (No. 422004582), and K. C. Wong Magna Fund in Ningbo University.

Author information

Authors and Affiliations

  1. Key Laboratory of Applied Marine Biotechnology, Ningbo University, Chinese Ministry of Education, 818 Fenghua Road, Ningbo, 315211, China

    Shujian Chen, Ce Shi, Yangfang Ye, Ronghua Li, Weiwei Song, Changkao Mu, Zhiming Ren & Chunlin Wang

  2. Marine Economic Research Center, Dong Hai Strategic Research Institute, Ningbo University, Ningbo University, 818 Fenghua Road, Ningbo, 315211, China

    Shujian Chen & Ce Shi

  3. Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, 818 Fenghua Road, Ningbo, 315211, China

    Shujian Chen, Ce Shi, Yangfang Ye, Ronghua Li, Weiwei Song, Changkao Mu, Zhiming Ren & Chunlin Wang

  4. Institute of Semiconductors, Chinese Academy of Sciences, Beijing, 100083, China

    Changbin Song

Authors
  1. Shujian Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ce Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yangfang Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ronghua Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Weiwei Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Changbin Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Changkao Mu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhiming Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chunlin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Shujian Chen performed the experiments and analyses and wrote the first draft of the manuscript; Ce Shi conceptualization and review and editing; Yangfang Ye contributed to the review and editing; Ronghua Li & Weiwei Song contributed to the review, editing, and supervision; Changkao Mu & Zhiming Ren contributed to animals’ resources; Chunlin Wang contributed to experimental design and funding acquisition.

Corresponding author

Correspondence to Ce Shi.

Ethics declarations

Ethics Approval

All animals used in the present study were conducted under the permission and supervision of the Institutional Animal Care and Use Committee of Ningbo University.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 748 KB)

Supplementary file2 (XLSX 69 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, S., Shi, C., Ye, Y. et al. Comparative Transcriptome Analysis Reveals the Light Spectra Affect the Growth and Molting of Scylla paramamosain by Changing the Chitin Metabolism. Mar Biotechnol 26, 351–363 (2024). https://doi.org/10.1007/s10126-024-10301-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-024-10301-3

Keywords

Search

Navigation