Ecological Archives A025-104-A3

Bharath Ananthasubramaniam, Edward McCauley, Kurt A. Gust, Alan J. Kennedy, Erik B. Muller, Edward J. Perkins, and Roger M. Nisbet. 2015. Relating suborganismal processes to exotoxological and population level endpoints using a bioenergetics model. Ecological Applications 25:16911710. http://dx.doi.org/10.1890/14-0498.1

Appendix C. Literature summary of papers investigating global transcript expression in Daphnia.

Our observations are arranged into five transcriptomics-based categories relevant to the DEB sensitivity analysis including: (1) Energy Utilization, (2) Oxygen Transport for Aerobic Respiration, (3) Feeding and Assimilation, (4) Carapace and Molting and (5) Reproduction. Further, the results are sorted against apical (organism level) effects on growth, reproduction or combined growth and reproduction effects to provide phenotypic anchoring for changes in gene transcript expression. (Particular effects on growth and reproduction are indicated in bold letters).

Table C1. Energy Utilization (Based on Transcript Expression Data).

Exposure

Apical Effect

Sub-Organismal Effect

Genomic Effect (Function)

Expression

Reference

Cd

Negative effects on Population Growth Rate (PGR) - Survivorship, Growth & Reproduction

Carbohydrate & Fat Metab (Glycoloysis / Gluconeogenesis)

increased

(Connon et al. 2008)

Cd

Negative effects on Population Growth Rate (PGR) - Survivorship, Growth & Reproduction

Energy Metabolism

mixed

(Connon et al. 2008)

Cd

Decreased Growth, Reproduction & Fitness - Length, Number of Clutches, Total neonates, Per Capita Birth Rate

Lipid-Ovary Index

Response to Metals Stress

increased

(Shaw et al. 2007)

P limited food

Negative effects on Growth

arachidonic acid metabolism

decreased

(Jeyasingh et al. 2011)

propiconazole

Negative effects on Growth & Juvenile Development

ATP Synthesis

increased

(Soetaert et al. 2006)

P limited food

Negative effects on Growth

biosynthesis of alkaloids derived from histidine and purine

increased

(Jeyasingh et al. 2011)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Carbohydrate Metabolism

increased

(Soetaert et al. 2007a)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Carbohydrate Metabolism

mixed

(Vandenbrouck et al. 2009)

Polar & Nonpolar Narcotics

Negative effects on Growth

Decreased caloric content: carbs, lipid, & protein

Carbohydrate Metabolism

mixed

(Dom et al. 2012)

P limited food

Negative effects on Growth

glycerolipid metabolism

increased

(Jeyasingh et al. 2011)

Polar & Nonpolar Narcotics

Negative effects on Growth

Decreased caloric content: carbs, lipid, & protein

Lipid binding / lipid transport

mixed

(Dom et al. 2012)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Lipid Metabolism (alpha-esterase)

increased

(Soetaert et al. 2007a)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Lipid Metabolism (Vitellogenin - embryo nutrition)

decreased

(Soetaert et al. 2007a)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Lipid Metabolism (Vitellogenin)

decreased

(Vandenbrouck et al. 2009)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Protein Metabolism

increased

(Vandenbrouck et al. 2009)

Polar & Nonpolar Narcotics

Negative effects on Growth

Decreased caloric content: carbs, lipid, & protein

Protein Metabolism

increased

(Dom et al. 2012)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Protein Metabolism (proteolysis)

mixed

(Soetaert et al. 2007a)

fungicide fenarimol

Negative effects on Growth & Embryo development

Protein Metabolism (Proteolysis)

increased

(Soetaert et al. 2007b)

propiconazole

Negative effects on Growth & Juvenile Development

Stress Response

mixed

(Soetaert et al. 2006)

P limited food

Negative effects on Growth

tryptophan metabolism

decreased

(Jeyasingh et al. 2011)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

Carbohydrate Metabolism

increased

(Heckmann et al. 2008)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

Lipid Metabolism

increased

(Heckmann et al. 2008)

Zn

Negative effects on Reproduction and juvenile growth

Lipid Transport, (All Vitellogenin-fused to SOD)

increased

(Vandegehuchte et al. 2010)

Zn

Negative effects on Reproduction and juvenile growth

Lipid Transport, (Vitellogenin)

decreased

(Vandegehuchte et al. 2010)

Zn

Negative effects on Reproduction and juvenile growth

Proteolysis

increased

(Vandegehuchte et al. 2010)

Cd

None measured - 1/10 LC50 Exposure

Fatty Acid Biosynthesis

decreased

(Poynton et al. 2011)

Cd

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Lipid Metabolism & Transport

decreased

(Poynton et al. 2008a)

Cu

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Lipid Metabolism & Transport

decreased

(Poynton et al. 2008b)

Zn

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

 

Lipid Metabolism & Transport

decreased

(Poynton et al. 2008a)

 

Table C2. Oxygen Transport for Aerobic Respiration (Based on Transcript Expression Data).

Exposure

Apical Effect

Sub-Organismal Effect

Genomic Effect (Function)

Expression

Reference

Cd

Decreased Growth, Reproduction & Fitness - Length, Number of Clutches, Total neonates, Per Capita Birth Rate

Lipid-Ovary Index

Oxygen Transport

increased

(Shaw et al. 2007)

Cd

Negative effects on Population Growth Rate (PGR) - Survivorship, Growth & Reproduction

Oxygen Transport

decreased

(Connon et al. 2008)

fungicide fenarimol

Negative effects on Growth & Embryo development

Oxygen Transport

increased

(Soetaert et al. 2007b)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Oxygen Transport

decreased

(Vandenbrouck et al. 2009)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Oxygen Transport (hemoglobin)

decreased

(Soetaert et al. 2007a)

Zn (dietary)

Negative effects on Reproduction (2nd brood onward), No effect on survival growth or feeding rate

Effect on time-to molt

Mitochondrial Function

increased

(De Schamphelaere et al. 2008)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

Oxidative phoshorylation

mixed

(Heckmann et al. 2008)

Zn

Negative effects on Reproduction and juvenile growth

Oxygen Transport (hemoglobin)

decreased

(Vandegehuchte et al. 2010)

Cd

None measured - 1/10 LC50 Exposure

Oxygen Transport

increased

(Poynton et al. 2011)

Cd

None measured - 1/10 LC50 Exposure

 

Oxygen Transport

increased

(Poynton et al. 2011)

 

Table C3. Feeding and Assimilation (Based on Transcript Expression Data).

Exposure

Apical Effect

Sub-Organismal Effect

Genomic Effect (Function)

Expression

Reference

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Digestion

increased

(Soetaert et al. 2007a)

fungicide fenarimol

Negative effects on Growth & Embryo development

Digestion & Nutrition Absorbtion

increased

(Soetaert et al. 2007b)

Dietary Differences

None measured

Gut Physiology

mixed

(Dudycha et al. 2012)

Cd

None measured - 1/10 LC50 Exposure

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2007)

Cu

None measured - 1/10 LC50 Exposure

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2007)

Zn

None measured - 1/10 LC50 Exposure

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2007)

Cd

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2008a)

Cu

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2008a)

Zn

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

 

Digestion & Nutrition Absorbtion

decreased

(Poynton et al. 2008a)

 

Table C4. Carapace and Molting (Based on Transcript Expression Data).

Exposure

Apical Effect

Sub-Organismal Effect

Genomic Effect (Function)

Expression

Reference

Cd

Negative effects on Population Growth Rate (PGR) - Survivorship, Growth & Reproduction

Chitin Metabolism

mixed

(Connon et al. 2008)

Cd

Decreased Growth, Reproduction & Fitness - Length, Number of Clutches, Total neonates, Per Capita Birth Rate

Lipid-Ovary Index

Chitin Metabollism

increased

(Shaw et al. 2007)

Cd

Negative effects on Population Growth Rate (PGR) - Survivorship, Growth & Reproduction

Cuticle Metabolism

mixed

(Connon et al. 2008)

Cd

Decreased Growth, Reproduction & Fitness - Length, Number of Clutches, Total neonates, Per Capita Birth Rate

Lipid-Ovary Index

Cuticle Protein metabolism

increased

(Shaw et al. 2007)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Chitin metabolism

increased

(Vandenbrouck et al. 2009)

Polar & Nonpolar Narcotics

Negative effects on Growth

Decreased caloric content: carbs, lipid, & protein

Cuticle Metabolism

mixed

(Dom et al. 2012)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Cuticle Metabolism (decreased at low Ni Conc, increased at high)

mixed

(Vandenbrouck et al. 2009)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Cuticle Protein metabolism

mixed

(Soetaert et al. 2007a)

fungicide fenarimol

Negative effects on Growth & Embryo development

Cuticle Protein metabolism

decreased

(Soetaert et al. 2007b)

propiconazole

Negative effects on Growth & Juvenile Development

Cuticle Protein Metabolism

mixed

(Soetaert et al. 2006)

Zn (dietary)

Negative effects on Reproduction (2nd brood onward), No effect on survival growth or feeding rate

Effect on time-to molt

Chitin Binding

decreased

(De Schamphelaere et al. 2008)

Zn

Negative effects on Reproduction and juvenile growth

Chitin Metabolism

mixed

(Vandegehuchte et al. 2010)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

Cuticle Metabolism

mixed

(Heckmann et al. 2008)

Zn (dietary)

Negative effects on Reproduction (2nd brood onward), No effect on survival growth or feeding rate

Effect on time-to molt

Cuticle Metabolism

decreased

(De Schamphelaere et al. 2008)

Cd

None measured - 1/10 LC50 Exposure

Chitin Metabolism

decreased

(Poynton et al. 2007)

Cu

None measured - 1/10 LC50 Exposure

Chitin Metabolism

mixed

(Poynton et al. 2007)

Zn

None measured - 1/10 LC50 Exposure

Chitin Metabolism

decreased

(Poynton et al. 2007)

Cd

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Chitin metabolism and cuticle metabolism

mixed

Poynton et al 2008

Cu

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Chitin metabolism and cuticle metabolism

mixed

(Poynton et al. 2008b)

Zn

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Chitin metabolism and cuticle metabolism

mixed

Poynton et al 2008

Cd

None measured - 1/10 LC50 Exposure

 

Cuticle Metabolism

increased

Poynton et al 2011

 

Table C5. Reproduction (Based on Transcript Expression Data).

Exposure

Apical Effect

Sub-Organismal Effect

Genomic Effect (Function)

Expression

Reference

P limited food

Negative effects on Growth

androgen and oestrogen metabolism

decreased

(Jeyasingh et al. 2011)

Polar & Nonpolar Narcotics

Negative effects on Growth

Decreased caloric content: carbs, lipid, & protein

Lipid binding / lipid transport (Vitellogenin)

mixed

(Dom et al. 2012)

fungicide fenarimol

Negative effects on Growth & Embryo development

Oogenesis - (Vitellogenin)

decreased

(Soetaert et al. 2007b)

Ni

Negative effects on Growth

Mixed effects on energy parameters: Hormesis @ low concentrations, negative effects at high: Available Energy (Carbohydrates, Protein & Lipid), Cellular Energy Allocation, Consumed Energy)

Oogenesis - (Vitellogenin)

decreased

(Vandenbrouck et al. 2009)

Cd

Negative effects on Growth

Negative effects on energy parameters: Cellular Energy Allocation, Energy Available (Protein, Carbohydrate & Lipid Reserves), Energy Consumed

Oogenesis and juvenile development (Vitellogenin)

decreased

(Soetaert et al. 2007a)

propiconazole

Negative effects on Growth & Juvenile Development

Oogenesis -Yolk Proteins & Vitellogenin

decreased

(Soetaert et al. 2006)

Zn (dietary)

Negative effects on Reproduction (2nd brood onward), No effect on survival growth or feeding rate

Effect on time-to molt

Chitin Binding

decreased

(De Schamphelaere et al. 2008)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

crustacean eicosanoid metabolism

mixed

(Heckmann et al. 2008)

Zn (dietary)

Negative effects on Reproduction (2nd brood onward), No effect on survival growth or feeding rate

Effect on time-to molt

Cuticle Metabolism

decreased

(De Schamphelaere et al. 2008)

Ibuprophen

Negative effects on Reproduction

Negative impacts on oogeneis and juvenile development

Oogenesis

decreased

(Heckmann et al. 2008)

Zn

Negative effects on Reproduction and juvenile growth

Oogenesis, (All Vitellogenin-fused to SOD)

increased

(Vandegehuchte et al. 2010)

Zn

Negative effects on Reproduction and juvenile growth

Oogenesis, (Vitellogenin)

decreased

(Vandegehuchte et al. 2010)

Cd

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Reproduction & Development

decreased

(Poynton et al. 2008a)

Cu

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

Reproduction & Development

decreased

(Poynton et al. 2008b)

Zn

None measured - 1/20 EC50, 1/10 EC50, 1/10 LC50, NOEC

 

Reproduction & Development

decreased

(Poynton et al. 2008a)

Literature cited

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Dom, N., L. Vergauwen, T. Vandenbrouck, M. Jansen, R. Blust, and D. Knapen. 2012. Physiological and Molecular Effect Assessment versus Physico-Chemistry Based Mode of Action Schemes: Daphnia magna Exposed to Narcotics and Polar Narcotics. Environmental Science & Technology 46:10–18.

Dudycha, J. L., C. S. Brandon, and K. C. Deitz. 2012. Population genomics of resource exploitation: insights from gene expression profiles of two Daphnia ecotypes fed alternate resources. Ecology and Evolution 2:329–340.

Heckmann, L.-H., R. M. Sibly, R. Connon, H. L. Hooper, T. H. Hutchinson, S. J. Maund, C. J. Hill, A. Bouetard, and A. Callaghan. 2008. Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biology 9:R40.

Jeyasingh, P. D., A. Ragavendran, S. Paland, J. A. Lopez, R. W. Sterner, and J. K. Colbourne. 2011. How do consumers deal with stoichiometric constraints? Lessons from functional genomics using Daphnia pulex. Molecular Ecology 20:2341–2352.

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Poynton, H. C., A. V. Loguinov, J. R. Varshavsky, S. Chan, E. J. Perkins, and C. D. Vulpe. 2008a. Gene Expression Profiling in Daphnia magna Part I: Concentration-Dependent Profiles Provide Support for the No Observed Transcriptional Effect Level. Environmental Science & Technology 42:6250–6256.

Poynton, H. C., J. R. Varshavsky, B. Chang, G. Cavigiolio, S. Chan, P. S. Holman, A. V. Loguinov, D. J. Bauer, K. Komachi, E. C. Theil, E. J. Perkins, O. Hughes, and C. D. Vulpe. 2007. Daphnia magna Ecotoxicogenomics Provides Mechanistic Insights into Metal Toxicity. Environmental Science & Technology 41:1044–1050.

Poynton, H. C., R. Zuzow, A. V. Loguinov, E. J. Perkins, and C. D. Vulpe. 2008b. Gene Expression Profiling in Daphnia magna, Part II: Validation of a Copper Specific Gene Expression Signature with Effluent from Two Copper Mines in California. Environmental Science & Technology 42:6257–6263.

De Schamphelaere, K. A. C., T. Vandenbrouck, B. T. A. Muyssen, A. Soetaert, R. Blust, W. De Coen, and C. R. Janssen. 2008. Integration of molecular with higher-level effects of dietary zinc exposure in Daphnia magna. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 3:307–314.

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Soetaert, A., L. N. Moens, K. Van der Ven, K. Van Leemput, B. Naudts, R. Blust, and W. M. De Coen. 2006. Molecular impact of propiconazole on Daphnia magna using a reproduction-related cDNA array. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 142:66–76.

Soetaert, A., T. Vandenbrouck, K. van der Ven, M. Maras, P. van Remortel, R. Blust, and W. M. De Coen. 2007a. Molecular responses during cadmium-induced stress in Daphnia magna: Integration of differential gene expression with higher-level effects. Aquatic Toxicology 83:212–222.

Soetaert, A., K. van der Ven, L. N. Moens, T. Vandenbrouck, P. van Remortel, and W. M. De Coen. 2007b. Daphnia magna and ecotoxicogenomics: gene expression profiles of the anti-ecdysteroidal fungicide fenarimol using energy-, molting- and life stage-related cDNA libraries. Chemosphere 67:60–71.

Vandegehuchte, M. B., T. Vandenbrouck, D. De Coninck, W. M. De Coen, and C. R. Janssen. 2010. Gene transcription and higher-level effects of multigenerational Zn exposure in Daphnia magna. Chemosphere 80:1014–1020.

Vandenbrouck, T., A. Soetaert, K. van der Ven, R. Blust, and W. De Coen. 2009. Nickel and binary metal mixture responses in Daphnia magna: Molecular fingerprints and (sub)organismal effects. Aquatic Toxicology 92:18–29.


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