Abstract
Background, aim and scope
There is growing evidence to show that dissolved humic substances, HSs, can directly interact with freshwater organisms, such as phototrophic organisms, cladocerans, amphipods and fish. The responses are—at least in part—transcriptionally controlled. These interactions can lead to stress symptoms in the exposed organisms. In phototrophs, stress symptoms include a reduction in photosynthetic oxygen release and antioxidative stress. Besides the direct effects, HSs also cause indirect effects that provoke different physiological adaptations in the phototrophs.
Materials and methods
The HS-influenced photosynthetic performance and stress response of two different green algae, Pseudokirchneriella subcapitata (Koršikov) Hindák and Monoraphidium braunii (Nägeli in Kützing) Komárková-Legnerová, and two cyanobacterial species, Synechocystis sp. (PCC 6803, Institut Pasteur) and Microcystis aeruginosa (PCC 7806, Institut Pasteur), were tested. Two humic preparations were applied, the synthetic HS1500 and HuminFeed®, HF, which had previously been proven effective in bioassays with invertebrates and a water mould.
Results and discussion
When the algae were grown near light saturation, most of the tested species were positively affected by HSs in growth rate or chlorophyll content. Cell sizes decreased with increasing HS concentrations for all eukaryotic phototrophs, except for the cyanobacteria. After 4 to 5 days of cultivation at the highest HS exposure, there was a decrease in total dry weight due to reduced cell sizes in contrast to an increase in cell numbers. With the exception of Synechocystis, the dry weight per cell ratio decreased with increasing HS concentration. The efficiency of utilizing absorbed light quanta increased with increasing HS concentrations; the maximum quantum yield of photosystem II (ΦPSIImax) was higher in all of the tested species, with the exception of M. aeruginosa, after exposure to HS.
Conclusion
The applied humic preparations did not interact directly with PSII, but changed the physiological state of the algae, especially the photosynthetic performance. Neither the green algae nor the cyanobacteria were inhibited in growth or negatively affected in their photosynthetic performance. The exposure to lower concentrations of HS stimulated better growth of the phototrophs. The tested humic preparations obviously did not have the potency to act as xenobiotic stressors; furthermore, there was no sign of herbicide potency.
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Notes
The use of HuminFeed® is not an advertisement for this product. For more information of this commercial product, the reader is referred to http://www.humintech.com/001/animalfeeds/products/huminfeed.html, accessed October 2010.
References
Ball AS, Williams M, Vincent D, Robinson J (2001) Algal growth control by a barley straw extract. Biores Technol 77:177–181
Bautista AIN, Necchi-Júnior O (2008) Photoacclimation in a tropical population of Cladophora glomerata (L.) Kützing 1843 (Chlorophyta) from southeastern Brazil. Braz J Biol 68(1):129–136
Bouchnak R, Steinberg CEW (2010) Modulation of longevity in Daphnia magna by food quality and simultaneous exposure to dissolved humic substances. Limnologica 40:86–91
Cazenave J, de los Ángeles Bistoni M, Zwirnmann E, Wunderlin DA, Wiegand C (2006) Attenuating effects of natural organic matter on microcystin toxicity in zebra fish (Danio rerio) embryos—benefits and costs of microcystin detoxication. Environ Toxicol 21:22–32
Euent S, Menzel R, Steinberg CEW (2008) Gender-specific lifespan modulation in Daphnia magna by a dissolved humic substances preparation. Ann Environ Sci 2:7–10
Everall NC, Lees DR (1996) The use of barley-straw to control general and blue-green algal growth in a Derbyshire reservoir. Wat Res 30:269–276
Falkowski PG (1984) Physiological responses of phytoplankton to natural light regimes. J Plankton Res 6(2):295–307
Ferrier MD, Butler BR, Terlizzi DE, Lacouture RV (2005) The effects of barley straw (Hordeum vulgare) on the growth of freshwater algae. Biores Technol 96:1788–1795
Giesy JP (2008) Stimulation of growth in Scenedesmus obliquus by humic acids under iron limited conditions. J Phycol 12:172–179
Gjessing ET, Alberts JJ, Bruchet A, Egeberg PK, Lydersen E, McGown LB, Mobed JJ, Münster U, Pempkowika J, Perdue M, Ratnawerra H, Rybacki D, Takacs M, Abbt-Braun G (1998) Multi-method characterisation of natural organic matter isolated from water: characterisation of reverse osmosis-isolates from water of two semi-identical dystrophic lakes basins in Norway. Water Res 32:3108–3124
Hoeffner SL, Manahan SE (1980) Influence of coal humic acid on the growth of Chlorella vulgaris. J Environ Sci 15:149–161
Imai A, Fukushima T, Matsushige K (1999) Effects of iron limitation and aquatic humic substances on the growth of Microcystis aeruginosa. Can J Fish Aquat Sci 56:1929–1937
Jackson TA, Hecky RE (1980) Depression of primary productivity by humic matter in lake and reservoir water of the boreal forest zone. Can J Fish Aquat Sci 37:2300–2317
Kamaya Y, Tsuboi S, Takada T, Suzuki K (2006) Growth stimulation and inhibition effects of 4-hydroxibenzoic acid and some related compounds on the freshwater green algae Pseudokirchneriella subcapitata. Arch Environ Contam Toxicol 51:537–541
Karasyova TA, Klose EO, Menzel R, Steinberg CEW (2007) Natural organic matter differently modulates growth of two closely related coccal green algal species. Environ Sci Poll Res 14:88–93
Körner S, Nicklisch A (2002) Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. J Phycol 38:862–871
Kullberg A, Bishop KH, Hargeby A, Jansson M, Petersen RC (1993) The ecological significance of dissolved organic-carbon in acidified waters. Ambio 22:331–337
Leenheer JA, Rostad CE (2004) Tannins and terpenoids as major precursors of Suwannee River fulvic acids. US Geological Survey Scientific Investigations Report 1004–5276. U.S. Geological Survey, Reston, p 16
Lichtenthaler HK, Rinderle U (1988) The role of chlorophyll fluorescence in the detection of stress conditions in plants. CRC Crit Rev Anal Chem 19(Suppl 1):29–85
Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC (1996) Humic substances as electron acceptors for microbial respiration. Nature 382:445–448
Malinsky-Rushansky N, Berman T, Berner T, Yacobi YZ, Dubinsky Z (2002) Physiological characteristics of picophytoplankton, isolated from Lake Kinneret: responses to light and temperature. J Plankton Res 24(11):1173–1183
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
McMaster D, Bond N (2008) A field and experimental study on the tolerance of fish to Eucalyptus camaldulensis leachate and low dissolved oxygen concentration. Mar Freshwat Res 59:177–185
Meinelt T, Phan TM, Zwirnmann E, Krüger A, Paul A, Wienke A, Steinberg CEW (2007) Reduction in vegetative growth of the water mold Saprolegnia parasitica (Coker) by humic substances of different origin. Aquat Toxicol 83:93–103
Menzel R, Stürzenbaum S, Bärenwaldt A, Kulas J, Steinberg CEW (2005) Humic material induces behavioral and global transcriptional responses in the nematode Caenorhabditis elegans. Environ Sci Technol 39:8324–8332
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Münster U (1985) Investigation about structure, distribution and dynamics of different organic substrates in the DOM of Lake Plusssee. Arch Hydrobiol Suppl 70:429–480
Nurnberg GK, Shaw M (1998) Productivity of clear and humic lakes: nutrients, phytoplankton, bacteria. Hydrobiologia 382:97–112
Ohkubo N, Yagi O, Okada M (1998) Effects of humic and fulvic acids on the growth of Microcystis aeruginosa. Environ Technol 19:611–617
Park MH, Han MS, Ahn CY, Kim HS, Yoon BD, Oh HM (2006) Growth inhibition of bloom forming cyanobacterium Microcystis aeruginosa by rice straw extract. Lett Appl Microbiol 43:307–312
Paul A, Pflugmacher S, Steinberg CEW (2003) Correlation of spin concentration in humic substances with inhibitory effects on photosynthesis of aquatic macrophytes. Akad gem Wissensch Erfurt, Sitzungsber Math-Naturw Klasse 12:209–221 (in German)
Pillinger JM, Cooper JA, Ridge I (1994) Role of phenolic compounds in the antialgal activity of barley straw. J Chem Ecol 20:1557–1569
Pörs Y, Wüstenberg A, Ehwald R (2010) A batch culture method for microalgae and cyanobacteria with CO2 supply through polyethylene membranes. J Phycol 46:825–830
Post AF, Dubinsky Z, Wyman Z, Falkowski PG (1984) Kinetics of light-intensity adaptation in a marine planktonic diatom. Marine Biol 83:231–238
Pouneva ID (2004) Effect of humic substances on the growth of microalgal cultures. Russ J Plant Physiol 52:410–413
Prokhotskaya VYu, Steinberg CEW (2007) Differential sensitivity of a coccal green algal and a cyanobacterial species to dissolved natural organic matter (NOM). Environ Sci Poll Res 14(SI):11–18
Ridge I, Pillinger JM (1996) Towards understanding the nature of algal inhibitors from barley straw. Hydrobiologia 340:301–305
Ridge I, Walters J, Street M (1999) Algal growth control by terrestrial leaf litter: a realistic tool? Hydrobiologia 395(396):173–180
Roháĉek K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29
Sachse A, Babenzien D, Ginzel G, Gelbrecht J, Steinberg CEW (2001) Characterization of dissolved organic carbon (DOC) in a dystrophic lake and an adjacent fen. Biogeochemistry 54:279–296
Sarvala J, Ilmavirta V, Paasivirta L, Salonen K (1981) The ecosystem of the oligotrophic Lake Pääjärvi 3. Secondary production and an ecological energy budget of the lake. Verh Intern Verein Limnol 21:422–427
Schagerl M, Müller B (2006) Acclimation of chlorophyll a and carotenoid levels to different irradiances in four freshwater cyanobacteria. J Plant Physiol 163:709–716
Skulberg OM (1967) Algal cultures as a means to assess the fertilizing influence of pollution. Wat Poll Control Fed, Washington, D.C., pp 113–127
Stanier RY (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35:171–205
Steinberg CEW (2003) Ecology of humic substances in freshwaters. determinants from geochemistry to ecological niches. Springer, Berlin
Steinberg CEW, Bach S (1996) Growth promotion of a groundwater fulvic acid in a bacterial/algae system. Acta Hydrochim Hydrobiol 24:98–100
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 12:391–401
Steinberg CEW, Kamara S, Prokhotskaya VYu, Manusadžianas L, Karasyova T, Timofeyev MA, Zhang J, Paul A, Meinelt T, Farjalla VF, Matsuo AYO, Burnison BK, Menzel R (2006) Dissolved humic substances—ecological driving forces from the individual to the ecosystem level? Freshwat Biol 51:1189–1210
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
Steinberg CEW, Meinelt T, Timofeyev MA, Bittner M, Menzel R (2008) Humic substances (review series). Part 2. Interactions with organisms. Environ Sci Poll Res 15:128–135
Steinberg CEW, Ouerghemmi N, Herrmann S, Bouchnak R, Timofeyev MA, Menzel R (2010a) Stress by poor food quality and exposure to humic substances: Daphnia magna responds with oxidative stress and lifespan extension. Hydrobiologia 652:223–236
Steinberg CEW, Vićentić L, Rauch R, Bouchnak R, Suhett AL, Menzel R (2010b) Exposure to humic material modulates life history traits of the cladocerans Moina macrocopa and M. micrura. Chem Ecol 26-S2:135–143
Suggett DJ, Floc’H EL, Harris GN, Leonardos N, Geider RJ (2007) Different strategies of photoacclimation by two strains of Emiliania huxleyi (Haptophyta). J Phycol 43:1209–1222
Suhett AL, Amado AM, Enrich-Prast A, Esteves FDA, Farjalla VF (2007) Seasonal changes of dissolved organic carbon photo-oxidation rates in a tropical humic lagoon: the role of rainfall as a major regulator. Can J Fish Aquat Sci 64:1266–1272
Suhett AL, Steinberg CEW, Santangelo JM, Bozelli RL, Farjalla VF (2011) Natural dissolved humic substances increase the lifespan and the salt stress resistance in the cladoceran species Moina macrocopa. Environ Sci Poll Res (in press)
Sun BK, Yasunori T, Hajime U (2005) Influences of iron and humic acid on the growth of the cyanobacterium Anabaena circinalis. Biochem Eng J 24:195–201
Sun BK, Tanji Y, Unno H (2006) Extinction of cells of cyanobacterium Anabaena circinalis in the presence of humic acid under light. Appl Microbiol Biotechnol 72:823–828
Vrana D, Votruba J (1995) Influence of soluble humic substances on the growth of algae and blue-green algae. Folia Microbiol 40:207–208
Wang WH, Bray CM, Jones MN (1999) The fate of 14C-labelled humic substances in rice cell in cultures. J Plant Physiol 154:203–211
Welch IM, Barrett PRF, Gibson MT, Ridge I (1990) Barley straw as an inhibitor of algae growth I: studies in the Chesterfield Canal. J Appl Phycol 2:231–239
Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic, San Diego, p 708
Acknowledgements
The help given by some people of the stress ecology laboratory is gratefully acknowledged, particularly by Shumon Chakrabati for assisting in the laboratory work, Andreas Nicklisch and Matthias Gilbert for general advices and Yvonne Poers and Ulrich Schreiber for advices with the Phyto-PAM. We also thank the Deutsche Forschungsgemeinschaft (DFG) for supporting the scientific work (Grant STE 673/17-1).
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Bährs, H., Steinberg, C.E.W. Impact of two different humic substances on selected coccal green algae and cyanobacteria—changes in growth and photosynthetic performance. Environ Sci Pollut Res 19, 335–346 (2012). https://doi.org/10.1007/s11356-011-0564-7
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DOI: https://doi.org/10.1007/s11356-011-0564-7