Effect of freeze-thaw cycles and 4-nonylphenol on cellular energy allocation in the freeze-tolerant enchytraeid Enchytraeus albidus

详细信息    查看全文

• 作者：Ana L. Patrício-Silva ; Mónica J. B. Amorim
• 关键词：Freeze tolerance ; Cellular energy allocation ; Energy budgets ; Freeze ; thaw cycles ; 4 ; Nonylphenol
• 刊名：Environmental Science and Pollution Research
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：23
• 期：4
• 页码：3548-3555
• 全文大小：789 KB
• 参考文献：Amorim MJB, Gomes SIL, Soares AMVM, Scott-Fordsmand JJ (2011) Energy basal levels and allocation among lipids, proteins, and carbohydrates in Enchytraeus albidus: changes related to exposure to Cu salt and Cu nanoparticles. Water Air Soil Pollut 223:477–482. doi:10.​1007/​s11270-011-0867-9 CrossRef
  Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH (1987) Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24(4):324–331. doi:10.​1016/​0011-2240(87)90036-8 CrossRef
  Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225. doi:10.​1146/​annurev-ento-112408-085356 CrossRef
  Bagheri F, Talebi K, Hosseininaveh V (2010) Cellular energy allocation of pistachio green stink bug, Brachynema germari Kol. (Hemiptera.: Pentatomidae) in relation to juvenoid pyriproxyfen. Afr J Biotechnol 9(35):5746–5753. doi:10.​5897/​AJB10.​674
  Bale JS, Worland MR, Block W (2001) Effects of summer frost exposures on the cold tolerance strategy of a sub-Antarctic beetle. J Insect Physiol 47(19):1161–1167. doi:10.​1016/​S0022-1910(01)00097-X CrossRef
  Belaiche C, Holt A, Saada A (2009) Nonylphenol ethoxylate plastic additives inhibit mitochondrial respiratory chain complex I. Clin Chem 55(19):1883–1884. doi:10.​1373/​clinchem.​2009.​130054 CrossRef
  Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37(8):911–7. doi:10.​1139/​o59-099 CrossRef
  Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.​1016/​0003-2697(76)90527-3 CrossRef
  Bragadin M, Perin G, Iero A, Manente S, Rizzoli V, Scutari G (1999) An in vitro study on the toxic effects of nonylphenols (NP) in mitochondria. Chemosphere 38(9):1997–2001. doi:10.​1016/​S0045-6535(98)00412-3 CrossRef
  Brown CL, Bale JS, Walters KFA (2004) Freezing induces a loss of freeze tolerance in an overwintering insect. Proc R Soc B 271:1507–1511. doi:10.​1098/​rspb.​2004.​2760 CrossRef
  Churchill TA, Storey KB (1989) Metabolic consequences of rapid cycles of temperature change for freeze-avoiding vs freeze-tolerant insects. J Insect Physiol 35(7):579–585. doi:10.​1016/​0022-1910(89)90147-9 CrossRef
  Crowe JH, Crowe LM, Carpenter JF, Aurell Wistrom C (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242:1–10CrossRef
  De Coen WM, Janssen CR (2003) The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ Toxicol Chem 22(7):1632–1641. doi:10.​1002/​etc.​5620220727 CrossRef
  De Coen WM, Janssen CR (1997) The use of biomarkers in Daphnia magna toxicity testing. IV Cellular energy allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia populations. J Aquat Ecosyst Stress Recover 6:43–55. doi:10.​1023/​A:​1008228517955 CrossRef
  Didden WAM (1993) Ecology of terrestrial Enchytraeidae. Pedobiologia 37:2–29
  Ekelund R, Granmo A, Magnusson K, Berggren M, Bergman A (1993) Biodegradation of 4-nonylphenol in seawater and sediment. Environ Pollut 79:59–61. doi:10.​1016/​0269-7491(93)90178-Q CrossRef
  Fisker KV, Holmstrup M, Malte H, Overgaard J (2014a) Effect of repeated freeze-thaw cycles on geographically different populations of the freeze-tolerant worm Enchytraeus albidus (Oligochaeta). J Exp Biol 217:3843–3852. doi:10.​1242/​jeb.​105650 CrossRef
  Fisker KV, Overgaard J, Sorensen JG, Slotsbo S, Holmstrup M (2014b) Roles of carbohydrate reserves for local adaptation to low temperatures in the freeze tolerant oligochaete Enchytraeus albidus. J Comp Physiol B 184(2):167–177. doi:10.​1007/​s00360-013-0788-6 CrossRef
  Giere O (2006) Ecology and biology of marine oligochaeta—an inventory rather than another review. Hydrobiologia 564:103–116. doi:10.​1007/​s10750-005-1712-1 CrossRef
  Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors aquatic and physiological applications. Springer Verlag, Berlin, Germany, pp 337–345CrossRef
  Hao C-j, Cheng X-j, Xia H-f, Ma X (2012) The endocrine disruptor 4-nonylphenol promotes adipocyte differenciation and induces obesity in mice. Cell Physiol Biochem 30:382–394. doi:10.​1159/​000339032 CrossRef
  Holmstrup M, Zachariassen KE (1996) Physiology of cold hardiness in earthworms. Comp Biochem Physiol A 115A(2):91–101. doi:10.​1016/​0300-9629(96)00010-2 CrossRef
  Holmstrup M, Bindesbøl A-M, Oostingh GJ, Duschl A, Scheil V, Kahler H-R, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408(18):3746–3762. doi:10.​1016/​j.​scitotenv.​2009.​10.​067 CrossRef
  Holmstrup M, Bouvrais H, Westh P, Wang C, Slotsbo S, Waagner D, Enggrob K, Ipsen JH (2014) Lipophilic contaminants influence cold tolerance of invertebrates through changes in cell membrane fluidity. Environ Sci Technol 48(16):9797–9803. doi:10.​1021/​es502221g CrossRef
  IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom, p 1535
  Jacobsen AMA, Mortensen GKG, Hansen HCBH (2004) Degradation and mobility of linear alkylbenzene sulfonate and nonylphenol in sludge-amended soil. J Environ Qual 33:232–240CrossRef
  Jänsch S, Amorim MJ, Römbke J (2005) Identification of the ecological requirements of important terrestrial ecotoxicological test species. Environ Rev 13(2):51–83. doi:10.​1139/​a05-007 CrossRef
  King FD, Packard TT (1975) Respiration and the activity of the respiratory electron transport system in marine zooplankton. Limnol Oceanogr 20:849–854. doi:10.​4319/​lo.​1975.​20.​5.​0849 CrossRef
  Lee RE, Dommel RA, Joplin KH, Denlinger DL (1995) Cryobiology of the freeze-tolerant gall fly Eurosta solidaginis: overwinteting energetics and heat shock proteins. Clim Res 5:61–67CrossRef
  Marshall KE, Sinclair BJ (2011) The sub-lethal effects of repeated freezing in the woolly bear caterpillar Pyrrharctia isabella. J Exp Biol 214(7):1205–1212. doi:10.​1242/​jeb.​054569 CrossRef
  Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35(6):971–986. doi:10.​1016/​j.​envint.​2009.​02.​006 CrossRef
  Novais SC, Amorim MJB (2013) Changes in cellular energy allocation in Enchytraeus albidus when exposed to dimethoate, atrazine, and carbendazim. Environ Toxicol Chem 32(12):2800–7. doi:10.​1002/​etc.​2368 CrossRef
  Novais SC, Soares AMVM, De Coen W, Amorim MJB (2013) Exposure of Enchytraeus albidus to Cd and Zn-Changes in cellular energy allocation (CEA) and linkage to transcriptional, enzymatic and reproductive effects. Chemosphere 90(3):1305–1309. doi:10.​1016/​j.​chemosphere.​2012.​09.​030 CrossRef
  Patricio Silva AL, Holmstrup M, Kostal V, Amorim MJB (2013) Soil salinity increases survival of freezing in the enchytraeid Enchytraeus albidus. J Exp Biol 216(Pt14):2732–2740. doi:10.​1242/​jeb.​083238 CrossRef
  Patricio Silva AL, Enggrob K, Slotsbo S, Amorim MJB, Holmstrup M (2014) Importance of freeze-thaw events in low temperature ecotoxicology of cold tolerant enchytraeids. Environ Sci Technol 48(16):9790–9796. doi:10.​1021/​es502161z CrossRef
  Patrício Silva AL, Amorim MJB, Holmstrup M (2015) Salinity changes impact of hazardous chemicals in Enchytraeus albidus. Environ Toxicol Chem 34(9):2159–2166. doi:10.​1002/​etc.​3058 CrossRef
  Ramløv H (2000) Aspects of natural cold tolerance in ectothermic animals. Hum Reprod 15:26–46CrossRef
  Shan J, Wang T, Li C, Klumpp E, Ji R (2010) Bioaccumulation and bound-residue formation of a branched 4-nonylphenol isomer in the geophagous earthworm Metaphire guillelmiin a rice paddy soil. Environ Sci Technol 44(12):4558–4563. doi:10.​1021/​es100139w CrossRef
  Sinclair BJ, Chown SL (2005) Deleterious effects of repeated cold exposure in a freeze-tolerant sub-Antarctic caterpillar. J Exp Biol 208(Pt5):869–879. doi:10.​1242/​jeb.​01455 CrossRef
  Slotsbo S, Maraldo K, Malmendal A, Nielsen NC, Holmstrup M (2008) Freeze tolerance and accumulation of cryoprotectants in the enchytraeid Enchytraeus albidus (Oligochaeta) from Greenland and Europe. Cryobiology 57(3):286–291. doi:10.​1016/​j.​cryobiol.​2008.​09.​010 CrossRef
  Smolders R, De Boeck G, Blust R (2003) Changes in cellular energy budget as a measure of whole effluent toxicity in zebrafish (Danio rerio). Environ Toxicol Chem 22:890–899CrossRef
  Smolders R, Bervoets L, De Coen W, Blust R (2004) Cellular energy allocation in zebra mussels exposed along a pollution gradient: linking cellular effects to higher levels of biological organization. Environ Pollut 129:99–112. doi:10.​1016/​j.​envpol.​2003.​09.​027 CrossRef
  Song YF, Luo Z, Pan YX, Liu X, Huang C, Chen QL (2014) Effects of copper and cadmium on lipogenic metabolism and metal element composition in the javelin goby (Synechogobius hasta) after single and combined exposure. Arch Environ Contam Toxicol 67(2):167–80. doi:10.​1007/​s00244-014-0011-0 CrossRef
  Verslycke T, Roast SD, Widdows J, Jones MB, Janssen CR (2004) Cellular energy allocation and scope for growth in the estuarine mysid Neomysis integer (Crustacea: Mysidacea) following chlorpyrifos exposure: a method comparison. J Exp Mar Biol Ecol 306:1–16. doi:10.​1016/​j.​jembe.​2003.​12.​022 CrossRef
  Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65(4):799–832
  
• 作者单位：Ana L. Patrício-Silva (1)
  Mónica J. B. Amorim (1)
  
  1. Department of Biology & CESAM (Centre for Environmental and Marine Studies), University of Aveiro, 3810-193, Aveiro, Portugal
  
• 刊物类别：Earth and Environmental Science
• 刊物主题：Environment
  Environment
  Atmospheric Protection, Air Quality Control and Air Pollution
  Waste Water Technology, Water Pollution Control, Water Management and Aquatic Pollution
  Industrial Pollution Prevention
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1614-7499

文摘

Due to climate change and intense anthropogenic activity, organisms from cold regions are often exposed to combined effects of temperature fluctuations and contaminants. In this investigation, we assessed the lipid, protein, and carbohydrate energy budgets; the energy available (Ea); consumed (Ec); and cellular energy allocation (CEA) of the freeze-tolerant Enchytraeus albidus, when exposed to sublethal concentrations of 4-nonylphenol (a lipophilic contaminant) for 7 days, followed by exposure to different temperature regimes (continuous 2 °C, continuous −4 °C, and daily freeze-thaw cycles (FTC) (2 to −4 °C) for additional 10 days. Results showed that a pre-exposure to 4-nonylphenol (4-NP) induced important changes in the worms’ energy budgets and CEA and increased mortality with most severe effects observed for the FTC events. For FTC, lipids were the most accumulated energy source, whereas during freezing (−4 °C), proteins were the most used. FTC caused the highest Ec, indicating the higher energy requirements for organisms when shifting between freezing and thawing events. This is also in line with the higher mortality observed in FTC compared to continuous −4 °C or 2 °C. Worms exposed to continuous freezing presented relatively stable and positive levels of Ea and low levels of Ec, possibly related with the decrease in metabolism. Keywords Freeze tolerance Cellular energy allocation Energy budgets Freeze-thaw cycles 4-Nonylphenol