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Genome-wide analysis of gene expression profile in the respiratory tree of sea cucumber (Apostichopus japonicus) in response to hypoxia conditions

  • Libin Zhang (a1) (a2), Qiming Feng (a1) (a2) (a3), Kui Ding (a1) (a2) (a3), Lina Sun (a1) (a2), Da Huo (a1) (a2) (a3), Yan Fang (a4), Tao Zhang (a1) (a2) and Hongsheng Yang (a1) (a2)...

Abstract

The sea cucumber Apostichopus japonicus is a deposit-feeder and vital for marine benthic ecosystems. Hypoxia can influence the behaviour and even lead to massive mortality in A. japonicus in the wild. It is important to understand the molecular responses of A. japonicus when exposed to acute changes in dissolved oxygen (DO) concentration. In this study, RNA-seq provided a general overview of the gene expression profiles of the respiratory tree of A. japonicus exposed to DO of 8 mg l−1 (DO8), 4 mg l−1 (DO4) and 2 mg l−1 (DO2) conditions. Differentially expressed genes (DEGs) screening with the NOISeq method identified 51, 59 and 61 DEGs according to the criteria of fold change ≥2 and divergence probability ≥0.8 in the comparisons of DO2 vs DO4, DO2 vs DO8 and DO4 vs DO8, respectively. Gene ontology analysis showed that ‘cellular process’ and ‘binding’ had the most enriched DEGs in the categories of ‘biological process’ and ‘molecular function’, respectively (catalytic activity also had the most enriched DEGs in the category of ‘molecular function’ based on the comparison of DO2 vs DO8), while ‘cell’ and ‘cell part’ had the most enriched DEGs in the category of ‘cellular component’. The DEGs were mapped to 79, 81 and 104 pathways in the KEGG database, and 8, 29 and 16 pathways were significantly enriched, respectively. The DO-specific DEGs identified in this study of the respiratory tree are important targets for further research into the biochemical mechanisms involved in the response of the sea cucumber to changes in the DO concentration.

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Corresponding author

Correspondence should be addressed to: H. Yang CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai Road, Qingdao 266071, China email: hshyang@qdio.ac.cn

References

Hide All
Abdi, H. (2007) The Bonferonni and Šidák corrections for multiple comparisons. Encyclopedia of Measurement and Statistics 3, 103107.
Deutsch, C., Brix, H., Ito, T., Frenzel, H. and Thompson, L. (2011) Climate-forced variability of ocean hypoxia. Science 333, 336339.
Diaz, R.J. (2001) Overview of hypoxia around the world. Journal of Environmental Quality 30, 275281.
Diaz, R.J. and Rosenberg, R. (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: An Annual Review 33, 245303.
Dong, Y., Dong, S. and Meng, X. (2008) Effects of thermal and osmotic stress on growth, osmoregulation and Hsp70 in sea cucumber (Apostichopus japonicus Selenka). Aquaculture 276, 179186.
Du, H., Bao, Z., Hou, R., Wang, S., Su, H., Yan, J., Tian, M., Li, Y., Wei, W., Lu, W., Hu, X., Wang, S. and Hu, J. (2012) Transcriptome sequencing and characterization for the sea cucumber Apostichopus japonicus (Selenka, 1867). PLoS ONE 7, e33311.
Eggermont, J. (2004) Calcium-activated chloride channels. Proceedings of the American Thoracic Society 1, 2227.
Gilliam, B.E., Reed, M.R., Chauhan, A.K., Dehlendorf, A.B. and Moore, T.L. (2011) Evidence of fibrinogen as a target of citrullination in IgM rheumatoid factor-positive polyarticular juvenile idiopathic arthritis. Pediatric Rheumatology 9, 110.
Gracey, A.Y., Troll, J.V. and Somero, G.N. (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proceedings of the National Academy of Sciences USA 98, 19931998.
Grantham, B.A., Chan, F., Nielsen, K.J. and Fox, D.S. (2004) Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429, 749754.
Gruber, A.D., Elble, R.C., Ji, H.-L., Schreur, K.D., Fuller, C.M. and Pauli, B.U. (1998) Genomic cloning, molecular characterization, and functional analysis of human CLCA1, the first human member of the family of Ca 2+-activated Cl channel proteins. Genomics 54, 200214.
Hemandezl, V., Robles, M. and Talon, M. (2006) Blast2GO goes grid: developing a grid-enabled prototype for functional genomics analysis. In Proceedings of the Challenges and Opportunities of Healthgrids: Proceedings of Healthgrid.
Holm, K., Hernroth, B. and Thorndyke, M. (2008) Coelomocyte numbers and expression of HSP70 in wounded sea stars during hypoxia. Cell and Tissue Research 334, 319325.
Kashenko, S. (2000) Acclimation of the sea cucumber Apostichopus japonicus to decreased salinity at the blastula and gastrula stages: its effect on the desalination resistance of larvae at subsequent stages of development. Russian Journal of Marine Biology 26, 422426.
Kim, D., Langmead, B. and Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12, 357360.
Kim, S.-H., Park, Y.-Y., Kim, S.-W., Lee, J.-S., Wang, D. and DuBois, R.N. (2011) ANGPTL4 induction by prostaglandin E2 under hypoxic conditions promotes colorectal cancer progression. Cancer Research 71, 70107020.
Kim, Y.K. and Jang, S.K. (2002) Continuous heat shock enhances translational initiation directed by internal ribosomal entry site. Biochemical and Biophysical Research Communications 297, 224231.
Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10, 1.
Lemaire, S.D. (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynthesis Research 79, 305318.
Li, B. and Dewey, C.N. (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 1.
Li, L. and Li, Q. (2010) Effects of stocking density, temperature, and salinity on larval survival and growth of the red race of the sea cucumber Apostichopus japonicus (Selenka). Aquaculture International 18, 447460.
Liao, Y. (1980) The aspidochirote holothurians of China with erection of a new genus. In Proceedings of the European Colloquium on Echinoderms, pp. 115120.
Meng, X., Dong, Y., Dong, S., Yu, S. and Zhou, X. (2011) Mortality of the sea cucumber, Apostichopus japonicus Selenka, exposed to acute salinity decrease and related physiological responses: osmoregulation and heat shock protein expression. Aquaculture 316, 8892.
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621628.
Nestlerode, J.A. and Diaz, R.J. (1998) Effects of periodic environmental hypoxia on predation of a tethered polychaete, Glycera americana: implications for trophic dynamics. Marine Ecology Progress Series 172, 185195.
Nilsson, H.C. and Sköld, M. (1996) Arm regeneration and spawning in the brittle star Amphiura filiformis (O.F. Müller) during hypoxia. Journal of Experimental Marine Biology and Ecology 199, 193206.
Oweson, C., Li, C., Söderhäll, I. and Hernroth, B. (2010) Effects of manganese and hypoxia on coelomocyte renewal in the echinoderm, Asterias rubens (L.). Aquatic Toxicology 100, 8490.
Pan, Y., Zhang, L., Lin, C., Sun, J., Kan, R. and Yang, H. (2015) Influence of flow velocity on motor behavior of sea cucumber Apostichopus japonicus. Physiology & Behavior 144, 5259.
Park, C.-I., Jung, J.-H., Shim, W.-J., Kim, J.-W., Kim, E.-G., Jeong, J.-M. and Kim, D.-H. (2012) Molecular characterization, expression, and functional analysis of two thioredoxins in the black rockfish (Sebastes schlegelii). Fish & Shellfish Immunology 32, 808815.
Ravetch, J.V. and Kinet, J.-P. (1991) Fc receptors. Annual Review of Immunology 9, 457492.
Ren, J.S., Stenton-Dozey, J. and Zhang, J. (2017) Parameterisation and application of dynamic energy budget model to sea cucumber Apostichopus japonicus. Aquaculture Environment Interactions 9, 18.
Shao, Y., Li, C., Ou, C., Zhang, P., Lu, Y., Su, X., Li, Y. and Li, T. (2013) Divergent metabolic responses of Apostichopus japonicus suffered from skin ulceration syndrome and pathogen challenge. Journal of Agricultural and Food Chemistry 61, 1076610771.
Shick, J.M. (1976) Physiological and behavioral responses to hypoxia and hydrogen sulfide in the infaunal asteroid Ctenodiscus crispatus. Marine Biology 37, 279289.
Siikavuopio, S.I., Dale, T., Mortensen, A. and Foss, A. (2007) Effects of hypoxia on feed intake and gonad growth in the green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266, 112116.
Sloan, N.A. (1984) Echinoderm fisheries of the world: a review. In Keegan, B.F. and O'Connor, B.D.S. (eds) Echinodermata. Rotterdam: A.A. Balkema Publishers, pp 109124.
Sui, J., Dong, S., Tian, X., Wang, F. and Dong, Y. (2010) The effect of light color on re spiration and excretion of sea cucumber, Apostichopus japonicus. Periodical of Ocean University of China 40, 6164. [In Chinese, with English abstract]
Sun, J., Zhang, L., Pan, Y., Lin, C., Wang, F., Kan, R. and Yang, H. (2015) Feeding behavior and digestive physiology in sea cucumber Apostichopus japonicus. Physiology & Behavior 139, 336343.
Sun, L., Chen, M., Yang, H., Wang, T., Liu, B., Shu, C. and Gardiner, D.M. (2011) Large scale gene expression profiling during intestine and body wall regeneration in the sea cucumber Apostichopus japonicus. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 6, 195205.
Sun, L., Yang, H., Chen, M., Ma, D. and Lin, C. (2013) RNA-Seq reveals dynamic changes of gene expression in key stages of intestine regeneration in the sea cucumber Apostichopus japonicus. PLoS ONE 8, e69441.
Tarazona, S., García-Alcalde, F., Dopazo, J., Ferrer, A. and Conesa, A. (2011) Differential expression in RNA-seq: a matter of depth. Genome Research 21, 22132223.
Theede, H., Ponat, A., Hiroki, K. and Schlieper, C. (1969) Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Marine Biology 2, 325337.
Vaquer-Sunyer, R. and Duarte, C.M. (2008) Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences USA 105, 1545215457.
Wang, F., Yang, H., Gao, F. and Liu, G. (2008) Effects of acute temperature or salinity stress on the immune response in sea cucumber, Apostichopus japonicus. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 151, 491498.
Wang, F., Yang, H., Wang, X., Xing, K. and Gao, F. (2011) Antioxidant enzymes in sea cucumber Apostichopus japonicus (Selenka) during aestivation. Journal of the Marine Biological Association of the United Kingdom 91, 209214.
Warner, J.R. and McIntosh, K.B. (2009) How common are extraribosomal functions of ribosomal proteins? Molecular Cell 34, 311.
Yuan, X., Yang, H., Wang, L., Zhou, Y. and Gabr, H.R. (2010) Effects of salinity on energy budget in pond-cultured sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea). Aquaculture 306, 348351.
Yuan, X., Yang, H., Wang, L., Zhou, Y., Zhang, T. and Liu, Y. (2007) Effects of aestivation on the energy budget of sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea). Acta Ecologica Sinica 27, 31553161.
Zhang, L., Pan, Y. and Song, H. (2015 a) Environmental drivers of behavior. In Yang, H., Hamel, J.-F. and Mercier, A. (eds) The sea cucumber Apostichopus japonicus: history, biology and aquaculture. Volume 39. Boston, MA: Academic Press, pp. 133152.
Zhang, L., Song, X., Hamel, J.-F. and Mercier, A. (2015 b) Aquaculture, stock enhancement, and restocking. In Yang, H., Hamel, J.-F. and Mercier, A. (eds) The sea cucumber Apostichopus japonicus: history, biology and aquaculture. Volume 39. Boston, MA: Academic Press, pp. 289322.
Zhang, P., Li, C., Zhang, P., Jin, C., Pan, D. and Bao, Y. (2014) iTRAQ-based proteomics reveals novel members involved in pathogen challenge in sea cucumber Apostichopus japonicus. PLoS ONE 9, e100492.
Zhang, P., Li, C., Zhu, L., Su, X., Li, Y., Jin, C. and Li, T. (2013) De novo assembly of the sea cucumber Apostichopus japonicus hemocytes transcriptome to identify miRNA targets associated with skin ulceration syndrome. PLoS ONE 8, e73506.
Zhao, Y., Yang, H., Storey, K.B. and Chen, M. (2014) Differential gene expression in the respiratory tree of the sea cucumber Apostichopus japonicus during aestivation. Marine Genomics 18, 173183.
Zhou, Z.C., Dong, Y., Sun, H.J., Yang, A.F., Chen, Z., Gao, S., Jiang, J.W., Guan, X.Y., Jiang, B. and Wang, B. (2014) Transcriptome sequencing of sea cucumber (Apostichopus japonicus) and the identification of gene-associated markers. Molecular Ecology Resources 14, 127138.

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Genome-wide analysis of gene expression profile in the respiratory tree of sea cucumber (Apostichopus japonicus) in response to hypoxia conditions

  • Libin Zhang (a1) (a2), Qiming Feng (a1) (a2) (a3), Kui Ding (a1) (a2) (a3), Lina Sun (a1) (a2), Da Huo (a1) (a2) (a3), Yan Fang (a4), Tao Zhang (a1) (a2) and Hongsheng Yang (a1) (a2)...

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