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Organic carbon source in formulated sediments influences life traits and gene expression of Caenorhabditis elegans

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Abstract

River water quality is strongly influenced by their sediments and their associated pollutants. To assess the toxic potential of sediments, sediment toxicity tests require reliable control sediments, potentially including formulated control sediments as one major option. Although some standardization has been carried out, one critical issue still remains the quality of sediment organic matter (SOM). Organic carbon not only binds hydrophobic contaminants, but may be a source of mild toxicity, even if the SOM is essentially uncontaminated. We tested two different sources of organic carbon and the mixture of both (Sphagnum peat (P) and one commercial humic substances preparation–HuminFeed®, HF) in terms of life trait variables and expression profiles of selected life performance and stress genes of the nematode Caenorhabditis elegans. In synchronous cultures, gene expression profiling was done after 6 and 48 h, respectively. The uncontaminated Sphagnum P reduced growth, but increased numbers of offspring, whereas HF did not significantly alter life trait variables. The 6 h expression profile showed most of the studied stress genes repressed, except for slight to strong induction in cyp-35B1 (all exposures), gst-38 (only mixture), and small hsp-16 genes (all exposures). After 48 h, the expression of almost all studied genes increased, particularly genes coding for antioxidative defense, multiple xenobiotic resistance, vitellogenin-like proteins, and genes regulating lifespan. Overall, even essentially uncontaminated SOM may induce several modes of action on the molecular level in C. elegans which may lead to false results if testing synthetic xenobiotics. This contribution is a plea for a strict standardization of the SOM quality in formulated sediments and to check for corresponding effects in other model sediment organisms, especially if using molecular toxicity endpoints.

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Notes

  1. http://www.humintech.com/049/animalfeeds/products/huminfeed.html (accessed May, 2011). See this site for more information. The use of HuminFeed® is because of pragmatical reasons and by no means an advertisement for this product.

References

  • Ankley GT, Benoit DA, Balogh JC, Reynoldson TB, Day KE, Hoke RA (1994) Evaluation of potential confounding factors in sediment toxicity tests with three freshwater benthic invertebrates. Environ Toxicol Chem 13(4):627–635

    Article  CAS  Google Scholar 

  • Baumeister R, Schaffitzel E, Hertweck M (2006) Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J Endocrinol 190(2):191–202

    Article  CAS  Google Scholar 

  • Bedulina DS, Timofeyev MA, Zimmer M, Zwirnmann E, Menzel R, Steinberg CEW (2010) Different natural organic matter isolates cause similar stress response patterns in the freshwater amphipod, Gammarus pulex. Environ Sci Poll Res 17(2):261–269

    Article  CAS  Google Scholar 

  • Besser JM, Brumbaugh WG, May TW, Ingersoll CG (2003) Effects of organic amendments on the toxicity and bioavailability of cadmium and copper in spiked formulated sediments. Environ Toxicol Chem 22(4):805–815

    Article  CAS  Google Scholar 

  • Bouchnak R, Steinberg CEW (2010) Modulation of longevity in Daphnia magna by food quality and simultaneous exposure to dissolved humic substances. Limnologica 40(2):86–91. doi:10.1016/j.limno.2009.11.010

    Article  CAS  Google Scholar 

  • Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71–94

    CAS  Google Scholar 

  • Brils J (2004) Sediment monitoring under the EU water framework directive. J Soils Sediment 4(2):72–73

    Article  Google Scholar 

  • Clément B, Devaux A, Perrodin Y, Danjean M, Ghidini-Fatus M (2004) Assessment of sediment ecotoxicity and genotoxicity in freshwater laboratory microcosms. Ecotoxicology 13(4):323–333

    Article  Google Scholar 

  • De Zwart D (2005) Impact of toxicity on species composition of aquatic communities: concordance of predictions and field observations. PhD Dissertation, University of Amsterdam, Amsterdam

  • Du Laing G, Rinklebe J, Vandecasteele B, Meers E, Tack FM (2009) Trace metal behaviour in estuarine and riverine floodplain soils and sediments—a review. Sci Total Environ 407(13):3972–3985. doi:10.1016/j.scitotenv.2008.07.025

    Article  CAS  Google Scholar 

  • ECHA (2008) Guidance on information requirements and chemical safety assessment. Chapter R.7b: endpoint specific guidance. vol guidance for the implementation of REACH. European Chemicals Agency, Helsinki

    Google Scholar 

  • Epel D (1998) Use of multidrug transporters as first lines of defense against toxins in aquatic organisms. Comp Biochem Physiol A 120(1):23–28. doi:10.1016/s1095-6433(98)10005-3

    Article  Google Scholar 

  • Glatzer H, Ahlf W (2001) Adjustment of a formulated sediment for sediment testing with Caenorhabditis elegans (Nematoda). Acta Hydrochim Hydrobiol 29(1):41–46

    Article  Google Scholar 

  • Goedkoop W, Peterson M (2003) The fate, distribution, and toxicity of lindane in tests with Chironomus riparius: effects of bioturbation and sediment organic matter content. Environ Toxicol Chem 22(1):67–76

    CAS  Google Scholar 

  • Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8(2):113–127

    Article  CAS  Google Scholar 

  • Haitzer M, Abbt-Braun G, Traunspurger W, Steinberg CEW (1999a) Effects of humic substances on the bioconcentration of polycyclic aromatic hydrocarbons: correlations with spectroscopic and chemical properties of humic substances. Environ Toxicol Chem 18(12):2782–2788

    Article  CAS  Google Scholar 

  • Haitzer M, Burnison BK, Höss S, Traunspurger W, Steinberg CEW (1999b) Effects of quantity, quality, and contact time of dissolved organic matter on bioconcentration of benzo[a]pyrene in the nematode Caenorhabditis elegans. Environ Toxicol Chem 18(3):459–465

    CAS  Google Scholar 

  • Harrington LA, Harley CB (1988) Effect of vitamin E on lifespan and reproduction in Caenorhabditis elegans. Mech Ageing Dev 43(1):71–78

    Article  CAS  Google Scholar 

  • Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, De la Cruz N, Davis P, Duesbury M, Fang R, Fernandes J, Han M, Kishore R, Lee R, Müller H, Nakamura C, Ozersky P, Petcherski A, Rangarajan A, Rogers A, Schindelman G, Schwarz EM, Tuli MA, Van Auken K, Wang D, Wang X, Williams G, Yook K, Durbin R, Stein LD, Spieth J, Sternberg PW (2010) Wormbase: a comprehensive resource for nematode research. Nucleic Acids Res 38(Suppl. 1):D463–D467

    Article  CAS  Google Scholar 

  • Haukås M, Ruus A, Hylland K, Berge JA, Mariussenyk E (2010) Bioavailability of hexabromocyclododecane to the polychaete Hediste diversicolor: exposure through sediment and food from a contaminated fjord. Environ Toxicol Chem 29(8):1709–1715

    Google Scholar 

  • Höss S, Haitzer M, Traunspurger W, Steinberg CEW (1999) Growth and fertility of Caenorhabditis elegans (Nematoda) in unpolluted freshwater sediments: response to particle size distribution and organic content. Environ Toxicol Chem 18(12):2921–2925

    Google Scholar 

  • Höss S, Bergtold M, Haitzer M, Traunspurger W, Steinberg CEW (2001) Refractory dissolved organic matter can influence the reproduction of Caenorhabditis elegans (Nematoda). Freshw Biol 46(1):1–10

    Article  Google Scholar 

  • Höss S, Ahlf W, Fahnenstich C, Gilberg D, Hollert H, Melbye K, Meller M, Hammers-Wirtz M, Heininger P, Neumann-Hensel H, Ottermanns R, Ratte HT, Seiler TB, Spira D, Weber J, Feiler U (2010) Variability of sediment-contact tests in freshwater sediments with low-level anthropogenic contamination—determination of toxicity thresholds. Environ Pollut 158(9):2999–3010

    Article  Google Scholar 

  • Ingersoll CG, Ankley GT, Benoit DA, Brunson EL, Burton GA, Dwyer EJ, Hoke RA, Landrum PE, Norberg-King TJ, Winger PV (1995) Toxicity and bioaccumulation of sediment-associated contaminants using freshwater invertebrates: a review of methods and applications. Environ Toxicol Chem 14(11):1885–1894

    Article  CAS  Google Scholar 

  • Ingersoll CG, Dillon T, Biddinger GR (1997) Ecological risk assessment of contaminated sediments. SETAC Press, Pensacola

    Google Scholar 

  • ISO (2010) Water quality-determination of the toxic effect of sediment and soil samples on growth, fertility and reproduction of Caenorhabditis elegans (Nematoda). International Organization for Standardization, Geneva

    Google Scholar 

  • Kampkötter A, Gombitang Nkwonkam C, Zurawski RF, Timpel C, Chovolou Y, Watjen W, Kahl R (2007) Effects of the flavonoids kaempferol and fisetin on thermotolerance, oxidative stress and FoxO transcription factor DAF-16 in the model organism Caenorhabditis elegans. Arch Toxicol 81(12):849–858. doi:10.1007/s00204-007-0215-4

    Article  Google Scholar 

  • Kemble NE, Dwyer FJ, Ingersoll CG, Dawson TD, Norberg-King TJ (1999) Tolerance of freshwater test organisms to formulated sediments for use as control materials in whole-sediment toxicity tests. Environ Toxicol Chem 18(2):222–230

    Article  CAS  Google Scholar 

  • Kirkwood TBL (1977) Evolution of ageing. Nature 270(5635):301–304

    Article  CAS  Google Scholar 

  • Lacey R, Watzin MC, McIntosh AW (1999) Sediment organic matter content as a confounding factor in toxicity tests with Chironomus tentans. Environ Toxicol Chem 18(2):231–236

    CAS  Google Scholar 

  • Lewis JA, Fleming JT (1995) Basic culture methods. In: Epstein HF, Shakes DC (eds) Caenorhabditis elegans: modern biological analysis of an organism. Academic Press, San Diego, pp 4–29

    Google Scholar 

  • Li XC, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253. doi:10.1146/annurev.ento.51.110104.151104

    Article  Google Scholar 

  • Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28(2):139–145

    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(4):402–408

    Article  CAS  Google Scholar 

  • Lundqvist A, Bertilsson S, Goedkoop W (2010) Effects of extracellular polymeric and humic substances on chlorpyrifos bioavailability to Chironomus riparius. Ecotoxicology 19(4):614–622

    Article  CAS  Google Scholar 

  • MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39(1):20–31

    Article  CAS  Google Scholar 

  • Macdonald RW, Harner T, Fyfe J (2005) Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data. Sci Total Environ 342(1–3):5–86

    CAS  Google Scholar 

  • Matsuo AYO, Woodin BR, Reddy CM, Val AL, Stegeman JJ (2006) Humic substances and crude oil induce cytochrome P450 1A expression in the Amazonian fish species Colossoma macropomum (Tambaqui). Environ Sci Technol 40(8):2851–2858. doi:10.1021/es052437i

    Article  CAS  Google Scholar 

  • Meems N, Steinberg CEW, Wiegand C (2004) Direct and interacting toxicological effects on the waterflea (Daphnia magna) by natural organic matter, synthetic humic substances and cypermethrin. Sci Total Environ 319(1–3):123–136. doi:10.1016/s0048-9697(03)00445-5

    CAS  Google Scholar 

  • Meinelt T, Paul A, Phan TM, Zwirnmann E, Krüger A, Wienke A, Steinberg CEW (2007) Reduction in vegetative growth of the water mold Saprolegnia parasitica (Coker) by humic substance of different qualities. Aquat Toxicol 83(2):93–103. doi:10.1016/j.aquatox.2007.03.013

    Article  CAS  Google Scholar 

  • Menzel R, Rödel M, Kulas J, Steinberg CE (2005a) CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch Biochem Biophys 438(1):93–102. doi:10.1016/j.abb.2005.03.020

    Article  CAS  Google Scholar 

  • Menzel R, Stürzenbaum S, Bärenwaldt A, Kulas J, Steinberg CEW (2005b) Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ Sci Technol 39(21):8324–8332

    Article  CAS  Google Scholar 

  • Menzel R, Swain SC, Hoess S, Claus E, Menzel S, Steinberg CE, Reifferscheid G, Sturzenbaum SR (2009) Gene expression profiling to characterize sediment toxicity—a pilot study using Caenorhabditis elegans whole genome microarrays. BMC Genomics 10:160. doi:10.1186/1471-2164-10-160

    Article  Google Scholar 

  • Morrow G, Battistini S, Zhang P, Tanguay RM (2004) Decreased lifespan in the absence of expression of the mitochondrial small heat shock protein Hsp22 in Drosophila. J Biol Chem 279(42):43382–43385

    Article  CAS  Google Scholar 

  • Naylor C, Rodrigues C (1995) Development of a test method for Chironomus riparius using a formulated sediment. Chemosphere 31(5):3291–3303

    Article  CAS  Google Scholar 

  • OECD (2004) Sediment-water chironomid toxicity test using spiked sediment, vol 218. Organisation for Economic Cooperation and Development, Paris

    Google Scholar 

  • Roman YE, De Schamphelaere KA, Nguyen LT, Janssen CR (2007) Chronic toxicity of copper to five benthic invertebrates in laboratory-formulated sediment: sensitivity comparison and preliminary risk assessment. Sci Total Environ 387(1–3):128–140. doi:10.1016/j.scitotenv.2007.06.023

    CAS  Google Scholar 

  • Rutkowski R, Dickinson R, Stewart G, Craig A, Schimpl M, Keyse SM, Gartner A (2011) Regulation of Caenorhabditis elegans p53/cep-1-dependent germ cell apoptosis by ras/MAPK signaling. PLoS Genet 7(8):e1002238

    Article  CAS  Google Scholar 

  • Saul N, Pietsch K, Menzel R, Steinberg CE (2008) Quercetin-mediated longevity in Caenorhabditis elegans: is DAF-16 involved? Mech Ageing Dev 129(10):611–613. doi:10.1016/j.mad.2008.07.001

    Article  CAS  Google Scholar 

  • Schmitt-Kopplin P, Hertkorn N, Schulten HR, Kettrup A (1998) Structural changes in a dissolved soil humic acid during photochemical degradation processes under O2 and N2 atmosphere. Environ Sci Technol 32(17):2531–2541. doi:10.1021/es970636z

    Article  CAS  Google Scholar 

  • Schwarzenberger A, Courts C, von Elert E (2009) Target gene approaches: gene expression in Daphnia magna exposed to predator-borne kairomones or to microcystin-producing and microcystin-free Microcystis aeruginosa. BMC Genomics 10:527

    Article  Google Scholar 

  • Selck H, Granberg ME, Forbes VE (2005) Impact of sediment organic matter quality on the fate and effects of fluoranthene in the infaunal brittle star Amphiura filiformis. Mar Environ Res 59(1):19–45

    Article  CAS  Google Scholar 

  • Spickermann W, Stork G (1986) Studies on sediments of the River Lahn 1. Analytical results. Fresenius Z Anal Chem 323(1):33–37. doi:10.1007/bf00531127

    Article  CAS  Google Scholar 

  • Steinberg CEW, Paul A, Pflugmacher S, Meinelt T, Klöcking R, Wiegand C (2003) Pure humic substances have the potential to act as xenobiotic chemicals—a review. Fresenius Environ Bull 12(5):391–401

    CAS  Google Scholar 

  • Steinberg CEW, Saul N, Pietsch K, Meinelt T, Rienau S, Menzel R (2007) Dissolved humic substances facilitate fish life in extreme aquatic environments and have the potential to extend lifespan of Caenorhabditis elegans. Ann Environ Sci 1:81–90

    CAS  Google Scholar 

  • Steinberg CEW, Vićentić L, Rauch R, Bouchnak R, Suhett AL, Menzel R (2010) Exposure to humic material modulates life history traits of the cladocerans Moina macrocopa and Moina micrura. Chem Ecol 26(Suppl 2):135–143

    Article  CAS  Google Scholar 

  • Sulston J, Hodgkin J (1988) Methods. In: Wood WB (ed) The nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory, Cold Spring Harbor, pp 587–606

    Google Scholar 

  • Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29(1):22–28

    Article  CAS  Google Scholar 

  • Timofeyev MA, Wiegand C, Burnison BK, Shatilina ZM, Pflugmacher S, Steinberg CEW (2004) Impact of natural organic matter (NOM) on freshwater amphipods. Sci Total Environ 319(1–3):115–121. doi:10.1016/s0048-9697(03)00444-3

    CAS  Google Scholar 

  • Timofeyev MA, Shatilina ZM, Kolesnichenko AV, Bedulina DS, Kolesnichenko VV, Pflugmacher S, Steinberg CE (2006) Natural organic matter (NOM) induces oxidative stress in freshwater amphipods Gammarus lacustris Sars and Gammarus tigrinus (Sexton). Sci Total Environ 366(2–3):673–681. doi:10.1016/j.scitotenv.2006.02.003

    CAS  Google Scholar 

  • US-EPA (2000) Methods for testing the toxicity and bioaccumulation of sediment-associated contaminants with freshwater invertebrates. U.S. Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Wedepohl KH (1995) The composition of the continental crust. Geochim Cosmoch Acta 59(7):1217–1232

    Article  CAS  Google Scholar 

  • Wisconsin-Department-of-Natural-Resources (2003) Consensus-based sediment quality-guidelines-recommendations for use & application-interim guidance. Wisconsin Department of Natural Resources, Madison, WI

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Acknowledgment

We gratefully acknowledge the support by the Deutsche Forschungsgemeinschaft, Grant STE 673-16/1 to R.M. The gifts of C. elegans and E. coli (OP50) from the Caenorhabditis Genetic Center (Theresa Stiernagle) are gratefully acknowledged.

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Authors and Affiliations

  1. Department of Biology, Humboldt-Universität zu Berlin, 12437, Berlin, Germany

    Julia Franzen, Ralph Menzel & Christian E. W. Steinberg

  2. Department of Ecology and Ecosystem Management, Technical University Munich, 85350, Freising-Weihenstephan, Germany

    Julia Franzen

  3. Institute of Biodiversity–Network (ibn), 93047 Regensburg & Ecossa (Ecological Sediment and Soil Assessment), 82319, Starnberg, Germany

    Sebastian Höss

  4. Department Biochemistry and Ecotoxicology, Federal Institute of Hydrology, 56068, Koblenz, Germany

    Evelyn Claus

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  1. Julia Franzen
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  2. Ralph Menzel
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  3. Sebastian Höss
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  5. Christian E. W. Steinberg
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Correspondence to Christian E. W. Steinberg.

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Franzen, J., Menzel, R., Höss, S. et al. Organic carbon source in formulated sediments influences life traits and gene expression of Caenorhabditis elegans . Ecotoxicology 21, 557–568 (2012). https://doi.org/10.1007/s10646-011-0816-9

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