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Photo-oxidation processes, properties of DOC, reactive oxygen species (ROS), and their potential impacts on native biota and carbon cycling in the Rio Negro (Amazonia, Brazil)

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Abstract

Given the reported degraded nature of DOC in the Rio Negro, and low oxygen, pH, and bacterial riverine levels, we hypothesized: (1) DOC would have strong humic and fulvic acid fluorescence signals with high aromaticity and large mean molecular weight; and (2) photo-oxidation rates would be slow, and reactive oxygen species (ROS) concentrations low, producing no oxidative stress in biota. We surveyed the environment and properties of DOC and explored DOC photo-oxidation and fish sensitivity to DOC products. DOC properties were investigated using absorption and fluorescence indices and parallel factor analysis (PARAFAC) of excitation–emission matrices. ROS concentrations were measured spectrophotometrically. A native fish, Hemigrammus levis, was exposed to photo-oxidizing DOC and its tissues (brain, gill, liver) assayed for changes in antioxidant and biotransformation enzymes. With respect to our hypotheses, (1) DOC was highly terrigenous, with high SAC340 values (aromaticity), high capacity to produce ROS, and high tryptophan-like fluorescence (bacterial, autochthonous signal); (2) photo-oxidation rates were appreciable, while products were related to mean UV-radiation levels (total radiation was constant). ROS levels were often higher than freshwater averages, yet fish experienced no oxidative stress. Results suggest photo-oxidation influences patterns in C-cycling, bacterial production and community dynamics between wet and dry seasons.

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References

  • Abele, D., B. Burlando, A. Viarengo & H.-O. Pörtner, 1998. Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comparative Biochemistry and Physiology Part B 120: 425–435.

    Article  Google Scholar 

  • Abele-Oeschger, D., H. Tüg & R. Rüdigers, 1997. Dynamics of UV-driven hydrogen peroxide formation on an intertidal sandflat. Limnology and Oceanography 42: 1406–1415.

    Article  CAS  Google Scholar 

  • Al Reasi, H. A., C. M. Wood & D. S. Smith, 2011. Physicochemical and spectroscopic properties of natural organic matter (NOM) from various sources and implications for ameliorative effects on metal toxicity to aquatic biota. Aquatic Toxicology 103: 179–190.

    Article  CAS  PubMed  Google Scholar 

  • Al Reasi, H. A., D. S. Smith & C. M. Wood, 2012. Evaluating the ameliorative effect of natural dissolved organic matter (DOM) quality on copper toxicity to Daphnia magna: improving the BLM. Ecotoxicology 21: 525–537.

    Article  Google Scholar 

  • Amado, L. L., M. L. Garcia, P. B. Ramos, R. F. Freitas, B. Zafalon, J. L. R. Ferreira, J. S. Yunes & J. M. Monserrat, 2009. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Science of the Total Environment 407: 2115–2123.

    Article  CAS  PubMed  Google Scholar 

  • Amon, R. M. W. & R. Benner, 1995. Photochemical and microbial consumption of dissolved organic carbon and dissolved oxygen in the Amazon River system. Geochimica et Cosmochimica Acta 60: 1783–1792.

    Article  Google Scholar 

  • Anderson, A., S. de Machado, C. M. Wood, A. Bianchini & P. L. Gillis, 2014. Responses of biomarkers in wild freshwater mussels chronically exposed to complex contaminant mixtures. Ecotoxicology 23: 1345–1358.

    Article  Google Scholar 

  • Araujo-Lima, C. A. R. M., L. P. S. Portugal & E. G. Ferreira, 1986. Fish-macrophyte relationship in the Anavilhanas Archipelago, a black water system in the Central Amazon. Journal of Fish Biology 29: 1–11.

    Article  Google Scholar 

  • Aucour, A.-M., F. X. Tao, P. Moreira-Tureq, P. Seyler, S. Sheppard & M. F. Benedetti, 2002. The Amazon River: behaviour of metals (Fe, Al, Mn) and dissolved organic matter in the initial mixing at the Rio Negro/Solimões confluence. Chemical Geology 197: 271–285.

    Article  Google Scholar 

  • Bastviken, D., L. J. Tranvik, J. A. Downing, P. M. Crill & A. Enrich-Prast, 2011. Freshwater methane emissions offset the continental carbon sink. Science 331: 50.

    Article  CAS  PubMed  Google Scholar 

  • Benner, R., S. Opsahl, G. Chin-Leo, J. E. Richey & B. R. Forsberg, 1995. Bacterial carbon metabolism in the Amazon River system. Limnology and Oceanography 40: 1262–1270.

    Article  Google Scholar 

  • Beutler, E., 1975. Red cell metabolism. A manual of biochemical methods. Grune & Stratton Inc., New York.

    Google Scholar 

  • Bradford, M., 1978. A rapid and sensitive method for the quantification of microgram quantities of protein, using the principle of protein-dye-binding. Analytical Biochemistry 72: 248–254.

    Article  Google Scholar 

  • Bruskov, V. I., L. V. Malakhova, Zh K Masalimov & A. V. Chernikov, 2002a. Heat induced reactive oxygen species and 8-oxoguanine, a biomarker of damage to DNA. Nucleic Acids Research 30: 1354–1360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruskov, V. I., Zh K Masalimov & A. V. Chernikov, 2002b. Heat-induced generation of reactive oxygen species in water. Doklady Biochemistry and Biophysics 384: 181–184.

    Article  CAS  PubMed  Google Scholar 

  • Cammack, W. K. L., J. Kalff, Y. T. Prairie & E. M. Smith, 2004. Fluorescent dissolved organic matter in lakes: relationships with heterotrophic metabolism. Limnology and Oceanography 49: 2034–2045.

    Article  Google Scholar 

  • Cooper, W. J., C. Shao, D. R. S. Lean, A. S. Gordon & F. E. Scully, 1994. Factors affecting the distribution of H,O, in surface waters. In Environmental Chemistry of Lakes and Reservoirs. Advances in Chemistry Series 237. American Chemical Society, pp. 393–422.

  • Cory, R. M. & D. M. McKnight, 2005. Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environmental Science and Technology 39: 8142–8149.

    Article  CAS  PubMed  Google Scholar 

  • Cory, R. M., C. P. Ward, B. C. Crump & G. W. Kling, 2014. Sunlight controls water column processing of carbon in arctic fresh waters. Science 345: 925–928.

    Article  CAS  PubMed  Google Scholar 

  • da Rosa, C. E., A. Bianchini & J. M. Monserrat, 2008. Antioxidant responses of Laeonereis acuta (Polychaeta) after exposure to hydrogen peroxide. Brazilian Journal of Medical and Biological Research 41: 117–121.

    Article  PubMed  Google Scholar 

  • Dahlén, J., S. Bertilsson & C. Petterson, 1996. Effects of UV-A irradiation on dissolved organic matter in humic surface waters. Environment International 22: 501–506.

    Article  Google Scholar 

  • Davis, E. S., 1986. Chromobacterium. In Braude, A. I., C. E. Davis & J. Fierer (eds), Infectious Diseases and Medical Microbiology, 2nd ed. WB Saunders, Philadelphia: 358–361.

    Google Scholar 

  • DePalma, G. S. S., W. R. Arnold, J. C. McGeer, D. G. Dixon & D. S. Smith, 2011. Variability in dissolved organic matter fluorescence and reduced sulfur concentration in coastal marine and estuarine environments. Applied Geochemistry 26: 394–404.

    Article  CAS  Google Scholar 

  • De Schamphelaere, K. A. C., F. M. Vasconcelos, F. M. G. Tack, H. E. Allen & C. R. Janssen, 2004. Effect of dissolved organic matter source on acute copper toxicity to Daphnia magna. Environmental Toxicology and Chemistry 23: 1248–1255.

    Article  PubMed  Google Scholar 

  • Determann, S., J. M. Lobbes, J. M. Reuter & J. Rullkotter, 1998. Ultraviolet fluorescence excitation and emission spectroscopy of marine algae and bacteria. Marine Chemistry 62: 137–156.

    Article  CAS  Google Scholar 

  • Draper, W. M. & D. G. Crosby, 1983. The photochemical generation of hydrogen peroxide in natural waters. Archives of Environmental Contamination and Toxicology 12: 121–126.

    Article  CAS  Google Scholar 

  • Durate, R. M., D. S. Smith, A. L. Val & C. M. Wood, 2016. Dissolved organic carbon from the upper Rio Negro protects zebrafish (Danio rerio) against ionoregulatory disturbances caused by low pH exposure. Scientific Reports 6: 20377. doi:10.1038/srep20377.

    Article  Google Scholar 

  • Duthie, P. B., P. Brando, G. P. Asner & C. B. Field, 2015. Projections of future meteorological drought and wet periods in the Amazon. Proceedings of the National Academy of Science 12: 13172–13177.

    Google Scholar 

  • Ertel, J. R., J. I. Hedges, A. H. Devol, J. E. Richey & M.-N. Góes-Ribeiro, 1986. Dissolved humic substances of the Amazon River system. Limnology and Oceanography 31: 739–754.

    Article  CAS  Google Scholar 

  • Fasching, C. & T. J. Battin, 2012. Exposure of dissolved organic matter to UV-radiation increases bacterial growth efficiency in a clear-water Alpine stream. Aquatic Sciences 74: 143–153.

    Article  CAS  Google Scholar 

  • Febria, C. M., L. F. W. Lesack, J. A. L. Gareis & M. L. Bothwell, 2006. Patterns of hydrogen peroxides among lakes of the Mackenzie Delta, western Canadian Arctic. Canadian Journal of Fisheries and Aquatic Sciences 63: 2107–2118.

    Article  CAS  Google Scholar 

  • Forsberg, B. R., A. H. Devol, J. E. Richey, L. A. Martinelli & H. dos Santos, 1988. Factors controlling nutrient conditions in Amazon floodplain lakes. Limnology & Oceanography 33: 41–56.

    Article  CAS  Google Scholar 

  • Galvez, F., A. Donini, R. C. Playle, S. Smith, M. O’Donnell & C. M. Wood, 2008. A matter of potential concern: natural organic matter alters the electrical properties of fish gills. Environmental Science and Technology 42: 9385–9390.

    Article  CAS  PubMed  Google Scholar 

  • Häkkinen, P. J., A. M. Anesio & W. Granéli, 2004. Hydrogen peroxide distribution, production, and decay in boreal lakes. Canadian Journal of Fisheries and Aquatic Sciences 61: 1520–1527.

    Article  Google Scholar 

  • Hopkins, J. & G. R. Tudhope, 1973. Glutathione peroxidase in human red cells in health and disease. Journal of Haematology 25: 563–575.

    Article  CAS  Google Scholar 

  • Huang, C.-C., Y.-M. Li, H. Yang, D.-Y. Sun, L.-J. Xu & X. Chen, 2013. Study of influencing factors to chromophoric dissolved organic matter absorption properties from fluorescence features in Taihu lake in autumn. Journal of Limnology 72: 326–335.

    Google Scholar 

  • Hudson, N., A. Baker & D. Reynolds, 2007. Fluorescence analysis of dissolved organic matter in natural, waste and polluted waters—a review. River Research and Applications 23: 631–649.

    Article  Google Scholar 

  • Huovinen, P. S., H. Penttilä & M. R. Soimasuo, 2003. Spectral attenuation of solar ultraviolet radiation in humic lakes in Central Finland. Chemosphere 51: 205–214.

    Article  CAS  PubMed  Google Scholar 

  • Johannsson, O. E., H. L. Bergman, C. M. Wood, P. Laurent, D. G. Kavembe, A. Bianchini, J. N. Maina, C. Chevalier, L. F. Bianchini, B. P. Michael & R. O. Ojoo, 2014. Air breathing in the Lake Magadi tilapia Alcolapia grahami, under normoxic and hyperoxic conditions, and the association with sunlight and ROS. Journal of Fish Biology 84: 844–863.

    Article  CAS  PubMed  Google Scholar 

  • Jordan, C. F. & R. Herrera, 1981. Tropical rain forests: are nutrients really critical? The American Naturalist 117: 167–180.

    Article  CAS  Google Scholar 

  • Keen, J. H., W. H. Habig & W. B. Jakoby, 1976. Mechanism for several activities of glutathione-S-transferase. Journal of Biological Chemistry 20: 6183–6188.

    Google Scholar 

  • Konhauser, K. O., W. F. Fyfe & B. I. Kronberg, 1994. Multi-element chemistry of some Amazonian waters and soils. Chemical Geology 111: 155–175.

    Article  Google Scholar 

  • Kumar, M. R., 2012. Chromobacterium violaceum: a rare bacterium isolated from a wound over the scalp. International Journal of Applied and Medical Research 2: 70–72.

    Google Scholar 

  • Küchler, I. L., N. Miekeley & B. R. Forsberg, 1994. Molecular mass distributions of dissolved organic carbon and associated metals in water from Rio Negro and Rio Solimões. The Science of the Total Environment 156: 207–216.

    Article  Google Scholar 

  • Kullberg, A., K. H. Bishop, A. Hargeby, M. Jansson & R. C. Peterson Jr, 1993. The ecological significance of dissolved organic carbon in acidified waters. Ambio 22: 331–337.

    Google Scholar 

  • Leenheer, J. A., 1980. Origin and nature of humic substances in the waters of the Amazon River basin. Acta Amazonica 10: 513–526.

    CAS  Google Scholar 

  • Lindell, M. J., W. Granéli & L. J. Tranvik, 1995. Enhanced bacterial growth in response to photochemical transformation of dissolved organic carbon. Limnology and Oceanography 40: 195–199.

    Article  Google Scholar 

  • Ma, X. & S. A. Green, 2004. Photochemical transformation of dissolved organic carbon in Lake Superior—An in-situ experiment. Journal of Great Lakes Research 30 Supplement 1: 97–112.

    Article  Google Scholar 

  • Matsuo, A. Y. O., C. M. Wood & A. L. Val, 2005. Effects of copper and cadmium on ion transport and gill metal binding in the Amazonian teleost tambaqui (Colossoma macropomum) in extremely soft water. Aquatic Toxicology 74: 351–364.

    Article  CAS  PubMed  Google Scholar 

  • McCord, J. E. & I. Fridovich, 1969. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry 244: 6049–6055.

    CAS  PubMed  Google Scholar 

  • McKnight, D. M., E. W. Boyer, P. K. Westerhoff, P. T. Doran, T. Kulbe & D. T. Anderson, 2001. Spectrofluorometric characterization of dissolved organic matter for indication of precursor organic material and aromaticity. Limnology and Oceanography 46: 38–48.

    Article  CAS  Google Scholar 

  • Miller, W. L. & D. R. Kester, 1994. Peroxide variations in the Sargasso Sea. Marine Chemistry 48: 17–29.

    Article  CAS  Google Scholar 

  • Molecular Probes, 2009. Amplex Ultra Red Reagent, Catalogue no. 36006.

  • Patel-Sorrentino, N., S. Mounier & J. Y. Benaim, 2002. Excitation–emission fluorescence matrix to study pH influence on organic matter fluorescence in the Amazon basin rivers. Water Research 36: 2571–2581.

    Article  CAS  PubMed  Google Scholar 

  • Patel-Sorrentino, N., S. Mounier, Y. Lucas & J. Y. Benaim, 2004. Effects of UV–visible irradiation on natural organic matter from the Amazon basin. Science of the Total Environment 321: 231–239.

    Article  CAS  PubMed  Google Scholar 

  • Rai, H. & G. Hill, 1982. Establishing the pattern of heterotrophic bacterial activity in three Central Amazonian lakes. Hydrobiologia 86: 121–126.

    Article  Google Scholar 

  • Roelke, D. L., J. B. Cotner, J. V. Montoya, C. E. Del Castillo, S. E. Davis, J. A. Snider, G. M. Gable & K. O. Winemiller, 2006. Optically determined sources of allochthonous organic matter and metabolic characterizations in a tropical oligotrophic river and associated lagoon. Journal of the North American Benthological Society 25: 185–197.

    Article  Google Scholar 

  • Ryan, A. C., E. J. Van Genderen, J. R. Tomasso & S. J. Klaine, 2004. Influence of natural organic matter source on copper toxicity to larval fathead minnows (Pimephales promelas): implications for the biotic ligand model. Environmental Toxicology and Chemistry 23: 1567–1574.

    Article  CAS  PubMed  Google Scholar 

  • Saint-Paul, U., 1996. Comparisons of seasonal and diurnal vertical oxygen distributions in central Amazonian white and black water lakes. Ecotropica 2: 73–77.

    Google Scholar 

  • Scully, N. M., D. J. McQueen, D. R. S. Lean & W. J. Cooper, 1996. Hydrogen peroxide formation: the interaction of ultraviolet radiation and dissolved organic carbon in lake waters along a 43–75°N gradient. Limnology and Oceanography 41: 540–548.

    Article  CAS  Google Scholar 

  • Scully, N. M., W. J. Cooper & L. J. Tranvik, 2003. Photochemical effects on microbial activity in natural waters: the interaction of reactive oxygen species and dissolved organic matter. FEMS Microbiology Ecology 46: 353–357.

    Article  CAS  PubMed  Google Scholar 

  • Steinberg, C. E. W., S. Kamara, V Yu Prokhotskaya, L. M. Ianas, T. A. Karasyova, M. A. Timofeyev, Z. Jie, A. Paul, T. Meinelt, V. F. Farjalla, A. Y. O. Matsuo, B. K. Burnison & R. Menzel, 2006. Dissolved humic substances – ecological driving forces from the individual to the ecosystem level? Freshwater Biology 21: 1189–1210.

    Article  Google Scholar 

  • Thurman, E. M., 1985. Organic Geochemistry of Natural Waters. Martinus Nijhoff/Dr. W. Junk Publishers, Dordrecht.

    Book  Google Scholar 

  • Timofeyev, M. A., C. Wiegand, B. K. Burnison, Z. M. Shatilina, S. Pflugmacher & C. E. W. Steinberg, 2004. Direct impact of natural organic matter (NOM) on freshwater amphipods. The Science of the Total Environment 319: 115–121.

    Article  CAS  PubMed  Google Scholar 

  • Tucker, A. J. & C. E. Williamson, 2011. Lakes in a new light: indirect effects of ultraviolet radiation. Freshwater Reviews 4: 115–134.

    Article  Google Scholar 

  • Val, A. L. & V. M. F. Almeida-Val, 1995. Fishes of the Amazon and Their Environment. Springer, Berlin.

    Book  Google Scholar 

  • Vigneault, B., A. Percot, M. LaFleur & P. C. G. Campbell, 2000. Permeability changes in model and phytoplankton membranes in the presence of aquatic humic substances. Environmental Science and Technology 34: 3907–3913.

    Article  CAS  Google Scholar 

  • Wetzel, R. G., 2001. Limnology. Lake and River Ecosystems, 3rd ed. Academic Press, San Diego, CA.

    Google Scholar 

  • Winters, A. R., T. A. E. Fish, R. C. Playle, D. S. Smith & P. J. Curtis, 2007. Photodegradation of natural organic matter from diverse freshwater sources. Aquatic Toxicology 84: 215–222.

    Article  Google Scholar 

  • Wissmar, R. C., J. E. Richey, R. F. Stallard & J. M. Edmond, 1981. Plankton metabolism and carbon processes in the Amazon River, its tributaries, and floodplain waters, Peru-Brazil, May–June 1977. Ecology 62: 1622–1633.

    Article  CAS  Google Scholar 

  • Wood, C. M., A. Y. O. Matsuo, R. W. Wilson, R. J. Gonzalez, M. L. Patrick, R. C. Playle & A. L. Val, 2003. Protection by natural blackwater against disturbances in ion fluxes caused by low pH exposure in freshwater stingrays endemic to the Rio Negro. Physiological Biochemical Zoology 76: 12–27.

    Article  PubMed  Google Scholar 

  • Wood, C. M., H. A. Al-Reasi & D. S. Smith, 2011. The two faces of DOC. Aquatic Toxicology 105S: 3–8.

    Article  Google Scholar 

  • Yan, M., G. V. Korshin, F. Claret, J.-P. Croue, M. Fabbricino, H. Gallard, T. Schäfer & M. F. Benedetti, 2014. Effects of charging on the chromophores of dissolved organic matter from the Rio Negro basin. Water Research 59: 154–164.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Many people have contributed to the success of this work, especially Maria de Nazaré de Paula da Silva and Vera Almeida Val who organized the expeditions and met our many requests. Others include Linda Diao—analysis of DOC samples, Rafael Duarte—assistance with the fish experiment, Gudrun De Boek—loan of her multimeter, Greg Goss—for sharing his UV data, Marcel de Paula Corrêa—for irradiance data, Sylvia Wood—maps in Fig. 1, Derek Campos—fish identification, Jeff Richards—logistical support, and Danielle McDonald—space to write at the Rosenstiel School of Marine and Atmospheric Sciences. Thank you all. Supported in Brazil by FAPEAM and CNPq through the ICT-ADAPTA grant to ALV and Ciência sem Fronteiras grant to ALV and CMW, and in Canada by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grants to CMW and DSS. CMW was supported by the Canada Research Chairs program.

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  1. Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Ora E. Johannsson & Chris M. Wood

  2. Department of Chemistry, Wilfrid Laurier University, Waterloo, ON, N2L 3C5, Canada

    D. Scott Smith & Giselle Cimprich

  3. Laboratório de Ecofisiologia e Evolução Molecular, Instituto Nacional de Pesquisas da Amazônia, INPA, Manaus, AM, Brazil

    Helen Sadauskas-Henrique & Adalberto L. Val

  4. Department of Biology, McMaster University, Hamilton, ON, L8S 4K1, Canada

    Chris M. Wood

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  1. Ora E. Johannsson
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Guest editors: Adalberto L. Val, Gudrun De Boeck & Sidinei M. Thomaz / Adaptation of Aquatic Biota of the Amazon

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Johannsson, O.E., Smith, D.S., Sadauskas-Henrique, H. et al. Photo-oxidation processes, properties of DOC, reactive oxygen species (ROS), and their potential impacts on native biota and carbon cycling in the Rio Negro (Amazonia, Brazil). Hydrobiologia 789, 7–29 (2017). https://doi.org/10.1007/s10750-016-2687-9

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