LC–MS/MS-Based Metabolome Analysis of Biochemical Pathways Altered by Food Limitation in Larvae of Ivory Shell, Babylonia areolata AuthorsAuthors and affiliations 17-22 phút
Jingqiang Fu Minghui Shen Yawei Shen Wengang Lü
Miaoqin Huang Xuan Luo Jinjin Yu Caihuan Ke
Jingqiang Fu o 1 o 2 Minghui Shen o 1 o 2 o 3 Yawei Shen o 1 o 2 Wengang Lü o 4 Miaoqin Huang o 1 o 2 Xuan Luo o 1 o 2 o 5 Jinjin Yu o 1
2 Caihuan Ke o 1 o 2 o 5 Weiwei You o 1 o 2 o 5 Email authorView author's OrcID profile
1. 1.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenPeople’s Republic of China 2. 2.College of Ocean and Earth SciencesXiamen UniversityXiamenPeople’s Republic of China 3. 3.Tropical Marine Products Fine Breed CenterHainan Academy of Ocean and Fisheries SciencesHainanPeople’s Republic of China 4. 4.College of FisheriesGuangdong Ocean UniversityZhanjiangPeople’s Republic of China 5. 5.Fujian Collaborative Innovation Center for Exploitation and Utilization of Marine Biological ResourcesXiamenPeople’s Republic of China Original Article First Online: 20 April 2018
Abstract Ivory shell, Babylonia areolata, is one of the commercially important mariculture species in China and South East Asia. Survival varies in the artificial hatching and larval rearing of B. areolata. Food deprivation may be involved in rearing mortality, and so, a better understanding of how larvae respond and adjust to starvation is needed. In this study, the metabolite profiles of newly hatched larvae with yolk (I), larvae with yolk exhaustion (II), larvae suffering 24 h starvation after yolk exhaustion (III), and larvae fed with exogenous nutrients after yolk exhaustion (IV) were analyzed by LC–MS/MS. Principal component and cluster analyses revealed differential abundance of metabolite profiles across groups. When compared to metabolite levels of the I group, significantly up-regulated metabolites included polyunsaturated fatty acids, phospholipids, nucleotide, amino acids, and their derivatives were found in the II group, indicating that organisms relied predominantly on glycerophospolipid metabolism and protein-based catabolism for energy production during this stage. During starvation after yolk exhaustion, the levels of all energy related metabolites were significantly reduced, but an increase in products of purine and pyrimidine metabolism indicated an insufficient energy supply and an increase in cellular disintegration. Larvae fed exogenous nutrients can have significantly improved metabolism compared to starved larvae. These findings suggest that metabolomics, using LC–MS/MS, can be used to assess the physiological status and food-affected metabolic changes affecting B. areolata larvae.
Keywords Babylonia areolata LC–MS/MS Metabolomics Newly hatched larvae Food limitation This is a preview of subscription content, log in to check access.
Notes Acknowledgements The authors thank the Hainan Academy of Ocean and Fisheries Sciences for its assistance in operations over the larval periods. This research was supported by the Earmarked Fund for Modern Agro-industry Technology Research System (No. CARS-48) and the Hainan Provincial Ocean Basic Budget Project in 2016.
References 1. Alfaro AC, Young T (2016) Showcasing metabolomic applications in aquaculture: a review. Rev Aquac 0:1–18Google Scholar 2. Baniasadi H, Vlahakis C, Hazebroek J, Zhong C, Asiago V (2014) Effect of environment and genotype on commercial maize hybrids using LC/MS-based metabolomics. J Agric Food Chem 62:1412–1422CrossRefPubMedGoogle Scholar 3. Benton HP, Ivanisevic J, Mahieu NG, Kurczy ME, Johnson CH, Franco L, Rinehart D, Valentine E, Gowda H, Ubhi BK, Tautenhahn R, Gieschen A, Field MW, Patti GJ, Siuzdak G (2015) Autonomous metabolomics for rapid metabolite identification in global profiling. Anal Chem 82:884–891CrossRefGoogle Scholar 4. Brunk UT, Svensson I (1999) Oxidative stress, growth factor starvation and Fas activation may all cause apoptosis through lysosomal leak. Redox Rep 4:3– 11CrossRefPubMedGoogle Scholar 5. Bulow FJ (1970) RNA–DNA ratios as indicators of recent growth rates of a fish. J Fish Res Board Can 27:2343–2349CrossRefGoogle Scholar 6. Calado R, Dionísio G, Dinis MT (2007) Starvation resistance of early zoeal stages of marine ornamental shrimps Lysmata spp. (Decapoda: Hippolytidae) from different habitats. J Exp Mar Biol Ecol 351:226–233CrossRefGoogle Scholar 7. Cetta CM, Capuzzo JM (1982) Physiological and biochemical aspects of embryonic and larval development of the winter flounder Pseudopleuronectes americanus. Mar Biol 71:327–337CrossRefGoogle Scholar 8. Chaitanawisuti N, Kritsanapuntu A, Natsukari Y, Kathinmai S (2001) Effects of feeding rates on the growth, survival and feed utilization of hatchery-reared juvenile spotted babylon Babylonia areolata Link 1807 in a flowthrough seawater system. Aquac Res 32:689–692CrossRefGoogle Scholar 9. Chaitanawisuti N, Kritsanapuntu S, Natsukari Y (2002) Economic analysis of a pilot commercial production for spotted babylon, Babylonia areolata (Link 1807), of marketable sizes using a flow-through culture system in Thailand. Aquac Res 33:1265– 1272CrossRefGoogle Scholar
10. Chen Y, Ke CH, Zhou SQ, Li FX (2004) Embryonic and larval development of Babylonia fonnosae habei (Altena and Gittenberger, 1981) (Gastropoda: Buccinidae) on China’s coast. Acta Oceanol Sin 23:521–531Google Scholar 11. Chen L, Zhou L, Chan ECY, Neo J, Beuerman RW (2011) Characterization of the human tear metabolome by LC–MS/MS. J Proteome Res 10:4876–4882CrossRefPubMedGoogle Scholar 12. Chen Y, Ke CH, Zhang SY, Dai XJ (2017) Feeding rate responses of Babylonia formosae habei (Prosobranchia: Buccinidae) larvae on cultured algae. Aquac Res 48:1538– 1549CrossRefGoogle Scholar 13. Compton MM (1992) A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Rev 11:105–119CrossRefPubMedGoogle Scholar 14. Crim RN, Sunday JM, Harley CDG (2011) Elevated seawater CO2 concentrations impair larval development and reduce larval survival in endangered northern abalone (Haliotis kamtschatkana). J Exp Mar Biol Ecol 400:272–277CrossRefGoogle Scholar 15. Cunha I, Conceição LEC, Planas M (2007) Energy allocation and metabolic scope in early turbot, Scophthalmus maximus, larvae. Mar Biol 151:1397–1405CrossRefGoogle Scholar 16. Dervishi E, Zhang GS, Dunn SM, Mandal R, Wishart DS, Ametaj BN (2017) GC–MS metabolomics identifies metabolite alterations that precede subclinical mastitis in the blood of transition dairy cows. J Proteome Res 16:433–446CrossRefPubMedGoogle Scholar 17. Dou SZ, Masuda R, Tanaka M, Tsukamoto K (2005) Effects of temperature and delayed initial feeding on the survival and growth of Japanese flounder larvae. J Fish Biol 66:362–377CrossRefGoogle Scholar 18. Ellis RP, Spicer JI, Byrne JJ, Sommer U, Viant MR, White DA, Widdicombe S (2014) 1H NMR metabolomics reveals contrasting response by male and female mussels exposed to reduced seawater pH, increased temperature, and a pathogen. Environ Sci Technol 48:7044–7052CrossRefPubMedGoogle Scholar 19. Feng JH, Li JQ, Wu HF, Chen Z (2013) Metabolic responses of HeLa cells to silica nanoparticles by NMR-based metabolomic analyses. Metabolomics 9:874– 886CrossRefGoogle Scholar 20. Finn RN, Fyhn HJ, Evjen MS (1995) Physiological energetics of developing embryos and yolk-sac larvae of Atlantic cod (Gadus morhua). I. Respiration and nitrogen metabolism. Mar Biol 124:355–369CrossRefGoogle Scholar 21. Fu JQ, Lü WG, Li WD, Shen MH, Luo X, Ke CH, You WW (2017) Comparative assessment of the genetic variation in selectively bred generations from two geographic populations of ivory shell (Babylonia areolata). Aquac Res 48:4205– 4218CrossRefGoogle Scholar 22. Giménez L (2002) Effects of prehatching salinity and initial larval biomass on survival and duration of development in the zoea 1 of the estuarine crab, Chasmagnathus granulata, under nutritional stress. J Exp Mar Biol Ecol 270:93–110CrossRefGoogle Scholar 23. González-Ortegón E, Giménez L, Blasco J, Le Vay L (2015) Effects of food limitation and pharmaceutical compounds on the larval development and morphology of Palaemon serratus. Sci Total Environ 503:171–178CrossRefPubMedGoogle Scholar
24. Guerao G, Simeó CG, Anger K, Urzúa Á, Rotllant G (2012) Nutritional vulnerability of early zoea larvae of the crab Maja brachydactyla (Brachyura, Majidae). Aquat Biol 16:253–264CrossRefGoogle Scholar 25. Heming TA, Buddington RK (1988) 6 yolk absorption in embryonic and larval fishes. Fish Physiol 11:407–446CrossRefGoogle Scholar 26. Holland DL, Spencer BE (1973) Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. J Mar Biol Assoc UK 53:287–298CrossRefGoogle Scholar 27. Houde ED (1974) Effects of temperature and delayed feeding on growth and survival of larvae of three species of subtropical marine fishes. Mar Biol 26:271– 285CrossRefGoogle Scholar 28. Ivanisevic J, Zhu ZJ, Plate L, Tautenhahn R, Chen S, O’Brien PJ, Johnson CH, Marletta MA, Patti GJ, Siuzdak G (2013) Toward ‘omic scale metabolite profiling: a dual separation–mass spectrometry approach for coverage of lipid and central carbon metabolism. Anal Chem 85:6876–6884CrossRefPubMedPubMedCentralGoogle Scholar 29. Jansson A, Norkko J, Norkko A (2013) Effects of reduced pH on Macoma balthica larvae from a system with naturally fluctuating pH-dynamics. PLoS One 8:e68198CrossRefPubMedPubMedCentralGoogle Scholar 30. Kelly AD, Breitkopf SB, Yuan M, Goldsmith J, Spentzos D, Asara JM (2011) Metabolomic profiling from formalin-fixed, paraffin-embedded tumor tissue using targeted LC/MS/MS: application in sarcoma. PLoS One 6:e25357CrossRefPubMedPubMedCentralGoogle Scholar 31. Krishnan P, Kruger NJ, Ratcliffe RG (2005) Metabolite fingerprinting and profiling in plants using NMR. J Exp Bot 56:255–265CrossRefPubMedGoogle Scholar 32. Kritsanapuntu S, Chaitanawisuti N, Natsukari Y (2007) Effects of different diets and seawater systems on egg production and quality of the broodstock Babylonia areolata L. under hatchery conditions. Aquac Res 38:1311–1316CrossRefGoogle Scholar 33. Kumlu M, Eroldogan OT, Aktas M (2000) Effects of temperature and salinity on larval growth, survival and development of Penaeus semisulcatus. Aquaculture 188:167– 173CrossRefGoogle Scholar 34. Lee SH, Woo HM, Jung BH, Lee J, Kwon OS, Pyo HS, Choi MH, Chung BC (2007) Metabolomic approach to evaluate the toxicological effects of nonylphenol with rat urine. Anal Chem 79:6102–6110CrossRefPubMedGoogle Scholar 35. Liu WG, Li Q, Gao FX, Kong LF (2010) Effect of starvation on biochemical composition and gametogenesis in the Pacific oyster Crassostrea gigas. Fish Sci 76:737– 745CrossRefGoogle Scholar 36. Liu R, Liang Y, Wu X, Xu D, Liu Y, Liu L (2011) First report on the detection of pectenotoxin groups in Chinese shellfish by LC–MS/MS. Toxicon 57:1000– 1007CrossRefPubMedGoogle Scholar 37. Lu CR, Shi Y, Wang Z, Song ZH, Zhu MC, Cai Q, Chen T (2008) Serum starvation induces H2AX phosphorylation to regulate apoptosis via p38 MAPK pathway. FEBS Lett 582:2703–2708CrossRefPubMedGoogle Scholar 38. Lü WG, Ke CH, Fu JQ, You WW, Luo X, Huang MQ, Yu JJ, Li WD, Shen MH (2016) Evaluation of crosses between two geographic populations of native Chinese and introduced Thai spotted ivory shell, Babylonia areolata, in southern China. J World Aquacult Soc 47:544–554CrossRefGoogle Scholar
39. Maity S, Jannasch A, Adamec J, Gribskov M, Nalepa T, Höök TO, Sepúlveda MS (2012) Metabolite profiles in starved Diporeia spp. using liquid chromatography–mass spectrometry (LC–MS) based metabolomics. J Crustac Biol 32:239–248CrossRefGoogle Scholar 40. Matias D, Joaquim S, Ramos M, Sobral P, Leitão A (2010) Biochemical compounds’ dynamics during larval development of the carpet-shell clam Ruditapes decussatus (Linnaeus, 1758): effects of mono-specific diets and starvation. Helgol Mar Res 65:369– 379CrossRefGoogle Scholar 41. McEdward LR, Qian PY (2001) Effects of the duration and timing of starvation during larval life on the metamorphosis and initial juvenile size of the polychaete Hydroides elegans (Haswell). J Exp Mar Biol Ecol 261:185–197CrossRefPubMedGoogle Scholar 42. Meyer B, Oettl B (2005) Effects of short-term starvation on composition and metabolism of larval Antarctic krill Euphausia superba. Mar Ecol Prog Ser 292:263– 270CrossRefGoogle Scholar 43. Millar RH, Scott JM (1967) The larva of the oyster Ostrea edulis during starvation. J Mar Biol Assoc UK 47:475–484CrossRefGoogle Scholar 44. Moran AL, Manahan (2004) Physiological recovery from prolonged ‘starvation’ in larvae of the Pacific oyster Crassostrea gigas. J Exp Mar Biol Ecol 306:17–36CrossRefGoogle Scholar 45. Ohkubo N, Matsubara T (2002) Sequential utilization of free amino acids, yolk proteins and lipids in developing eggs and yolk-sac larvae of barfin flounder Verasper moseri. Mar Biol 140:187–196CrossRefGoogle Scholar 46. Ohkubo N, Sawaguchi S, Hamatsu T, Matsubara T (2006) Utilization of free amino acids, yolk proteins and lipids in developing eggs and yolk-sac larvae of walleye pollock Theragra chalcogramma. Fish Sci 72:620–630CrossRefGoogle Scholar 47. Ohkubo N, Sawaguchi S, Nomura K, Tanaka H, Matsubara T (2008) Utilization of free amino acids, yolk protein and lipids in developing eggs and yolk-sac larvae of Japanese eel Anguilla japonica. Aquaculture 282:130–137CrossRefGoogle Scholar 48. Olson RR, Olson MH (1989) Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Annu Rev Ecol Syst 20:225– 247CrossRefGoogle Scholar 49. Pechenik JA, Cerulli TR (1991) Influence of delayed metamorphosis on survival, growth, and reproduction of the marine polychaete Capitella sp. I. J Exp Mar Biol Ecol 151:17– 27CrossRefGoogle Scholar 50. Roberts RD, Lapworth C, Barker RJ (2001) Effect of starvation on the growth and survival of post-larval abalone (Haliotis iris). Aquaculture 200:323–338CrossRefGoogle Scholar 51. Rønnestad I, Groot EP, Fyhn HJ (1993) Compartmental distribution of free amino acids and protein in developing yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus). Mar Biol 116:349–354CrossRefGoogle Scholar 52. Rønnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177:201–216CrossRefGoogle Scholar 53. Sánchez-Lazo C, Martínez-Pita I (2012) Biochemical and energy dynamics during larval development of the mussel Mytilus galloprovincialis (Lamarck, 1819). Aquaculture 358– 359:71–78Google Scholar
54. Sheedy JR, Lachambre S, Gardner DK, Day RW (2016) 1H-NMR metabolite profiling of abalone digestive gland in response to short-term starvation. Aquac Int 24:503– 521CrossRefGoogle Scholar 55. Staton JL, Sulkin SD (1991) Nutritional requirements and starvation resistance in larvae of the brachyuran crabs Sesarma cinereum (Bosc) and S. reticulatum (Say). J Exp Mar Biol Ecol 152:271–284CrossRefGoogle Scholar 56. Sun XJ, Li Q (2014) Effects of delayed first feeding on larval growth, survival and development of the sea cucumber Apostichopus japonicus (Holothuroidea). Aquac Res 45:278–288CrossRefGoogle Scholar 57. Suzuki M, Nishiumi S, Kobayashi T, Azuma T, Yoshida M (2016) LC–MS/MS-based metabolome analysis detected changes in the metabolic profiles of small and large intestinal adenomatous polyps in ApcMin/+ mice. Metabolomics 12:68CrossRefGoogle Scholar 58. Takamatsu M, Fujita T, Hotta H (2001) Suppression of serum starvation-induced apoptosis by hepatitis C virus core protein. Kobe J Med Sci 47:97–112PubMedGoogle Scholar 59. Viant MR, Rosenblum ES, Tjeerdema RS (2003) NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism health. Environ Sci Technol 37:4982–4989CrossRefPubMedGoogle Scholar 60. Vidal ÉAG, DiMarco P, Lee P (2006) Effects of starvation and recovery on the survival, growth and RNA/DNA ratio in loliginid squid paralarvae. Aquaculture 260:94– 105CrossRefGoogle Scholar 61. Wagner M, Durbin E, Buckley L (1998) RNA:DNA ratios as indicators of nutritional condition in the copepod Calanus finmarchicus. Mar Ecol Prog Ser 162:173– 181CrossRefGoogle Scholar 62. Want EJ, Cravatt BF, Siuzdak G (2005) The expanding role of mass spectrometry in metabolite profiling and characterization. Chembiochem 6:1941– 1951CrossRefPubMedGoogle Scholar 63. Wu HF, Zhang XY, Wang Q, Li LZ, Ji CL, Liu XL, Zhao JM, Yin XL (2013) A metabolomic investigation on arsenic-induced toxicological effects in the clam Ruditapes philippinarum under different salinities. Ecotoxicol Environ Saf 90:1– 6CrossRefPubMedGoogle Scholar 64. Wu XG, Zeng CS, Southgate PC (2016) Effects of starvation on survival, biomass, and lipid composition of newly hatched larvae of the blue swimmer crab, Portunus pelagicus (Linnaeus, 1758). Aquac Int 25:447–461CrossRefGoogle Scholar 65. Xia JG, Broadhurst DI, Wilson M, Wishart DS (2013) Translational biomarker discovery in clinical metabolomics: an introductory tutorial[J]. Metabolomics 9:280– 299CrossRefPubMedGoogle Scholar 66. Xiao JF, Varghese RS, Zhou B, Nezami Ranjbar MR, Zhao Y, Tsai TH, Poto CD, Wang JL, Goerlitz D, Luo Y, Cheema AK, Sarhan N, Soliman H, Tadesse MG, Ziada DH, Ressom HW (2012) LC–MS based serum metabolomics for identification of hepatocellular carcinoma biomarkers in Egyptian cohort. J Proteome Res 11:5914– 5923CrossRefPubMedPubMedCentralGoogle Scholar 67. Yan XW, Zhang YH, Huo ZM, Yang F, Zhang GF (2009) Effects of starvation on larval growth, survival, and metamorphosis of Manila clam Ruditapes philippinarum. Acta Ecol Sin 29:327–334CrossRefGoogle Scholar
68. Yandi I, Altinok I (2014) Defining the starvation potential and the influence on RNA/DNA ratios in horse mackerel (Trachurus mediterraneus) larvae. Helgol Mar Res 69:25–35CrossRefGoogle Scholar 69. Yokota T, Nakagawa T, Murakami N, Chimura M, Tanaka H, Yamashita Y, Funamoto T (2016) Effects of starvation at the first feeding stage on the survival and growth of walleye pollock Gadus chalcogrammus larvae. Fish Sci 82:73–83CrossRefGoogle Scholar 70. Young T, Alfaro AC, Villas-Bôas S (2015) Identification of candidate biomarkers for quality assessment of hatchery-reared mussel larvae via GC/MS-based metabolomics. New Zeal J Mar Fresh 49:87–95CrossRefGoogle Scholar 71. Yúfera M, Darias MJ (2007) The onset of exogenous feeding in marine fish larvae. Aquaculture 268:53–63CrossRefGoogle Scholar 72. Zhang CS, Li ZG, Li FH, Xiang JH (2015) Effects of starvation on survival, growth and development of Exopalaemon carinicauda larvae. Aquac Res 46:2289– 2299CrossRefGoogle Scholar 73. Zheng HP, Ke CH, Zhou SQ, Li FX (2005) Effects of starvation on larval growth, survival and metamorphosis of ivory shell Babylonia formosae habei Altena et al., 1981 (Neogastropoda: Buccinidae). Aquaculture 243:357–366CrossRefGoogle Scholar 74. Zheng HP, Ke CH, Sun ZW, Zhou SQ, Li FX (2010) Effects of stocking density and algal concentration on the survival, growth and metamorphosis of Bobu ivory shell, Babylonia formosae habei (Neogastropoda:Buccinidae) larvae. Aquac Res 42:1– 8CrossRefGoogle Scholar