A mesocosm-based study was conducted to assess the effect of glucose and hydrogen peroxide on periphyton communities. These chemicals have been found to be effective at controlling cyanobacteria blooms in the water column but their impact on attached communities is unknown. The experimental design included a total of 4 treatments: control (no chemicals; 3 replicates); hydrogen peroxide (3 replicates); glucose alone (3 different concentrations [no replicates]); and additive glucose (3 replicates). After 34 days, mean values of chlorophyll a were lower in all experimental treatments compared to the control; mean AFDM values were lower in all treatments except the unreplicated high glucose alone treatment. In contrast, mean autotrophic index values (AFDM/chlorophyll a) were greater in all treatments compared to the control, indicating heterotrophs were more resistant to the chemical treatments than autotrophs. Periphyton community biodiversity was much lower in the additive glucose and moderate glucose alone treatments than the hydrogen peroxide and control treatments. The relative abundance of the bacteria Asticcacaulis and Sphingorhabdus responded positively to the glucose treatments, whereas relative abundance of Nevskia and Caenimonas declined in both the hydrogen peroxide and glucose treatments. In terms of relative abundance, no cyanobacteria taxa were detected among the top 20 taxa. We conclude that the autotrophic component of periphyton communities is especially vulnerable to hydrogen peroxide and glucose treatments, and that any management strategy employing these chemicals should be aware of this potential impact.
References
[1]
Vadeboncoeur, Y. and Steinman, A.D. (2002) Periphyton Function in Lake Ecosystems. TheScientificWorldJournal, 2, 1449-1468. https://doi.org/10.1100/tsw.2002.294
[2]
Vadeboncoeur, Y., Peterson, G., Vander Zanden, M.J. and Kalff, J. (2008) Benthic Algal Production across Lake Size Gradients: Interactions among Morphometry, Nutrients, and Light. Ecology, 89, 2542-2552. https://doi.org/10.1890/07-1058.1
[3]
Vesterinen, J., Devlin, S.P., Syväranta, J. and Jones, R.I. (2017) Influence of Littoral Periphyton on Whole‐Lake Metabolism Relates to Littoral Vegetation in Humic Lakes. Ecology, 98, 3074-3085. https://doi.org/10.1002/ecy.2012
[4]
Gushulak, C.A.C., Haig, H.A., Kingsbury, M.V., Wissel, B., Cumming, B.F. and Leavitt, P.R. (2021) Effects of Spatial Variation in Benthic Phototrophs along a Depth Gradient on Assessments of Whole‐Lake Processes. FreshwaterBiology, 66, 2118-2132. https://doi.org/10.1111/fwb.13820
[5]
Wilkinson, G.M., Walter, J.A., Buelo, C.D. and Pace, M.L. (2021) No Evidence of Widespread Algal Bloom Intensification in Hundreds of Lakes. FrontiersinEcologyandtheEnvironment, 20, 16-21. https://doi.org/10.1002/fee.2421
[6]
Hou, X., Feng, L., Dai, Y., Hu, C., Gibson, L., Tang, J., et al. (2022) Global Mapping Reveals Increase in Lacustrine Algal Blooms over the Past Decade. NatureGeoscience, 15, 130-134. https://doi.org/10.1038/s41561-021-00887-x
[7]
Hallegraeff, G.M., Anderson, D.M., Belin, C., Bottein, M.D., Bresnan, E., Chinain, M., et al. (2021) Perceived Global Increase in Algal Blooms Is Attributable to Intensified Monitoring and Emerging Bloom Impacts. CommunicationsEarth&Environment, 2, Article ID: 117. https://doi.org/10.1038/s43247-021-00178-8
Jeppesen, E., Søndergaard, M., Jensen, J.P., Havens, K.E., Anneville, O., Carvalho, L., et al. (2005) Lake Responses to Reduced Nutrient Loading—An Analysis of Contemporary Long‐Term Data from 35 Case Studies. FreshwaterBiology, 50, 1747-1771. https://doi.org/10.1111/j.1365-2427.2005.01415.x
[10]
Beutel, M.W. and Horne, A.J. (1999) A Review of the Effects of Hypolimnetic Oxygenation on Lake and Reservoir Water Quality. LakeandReservoirManagement, 15, 285-297. https://doi.org/10.1080/07438149909354124
[11]
Jeppesen, E., Meerhoff, M., Jacobsen, B.A., Hansen, R.S., Søndergaard, M., Jensen, J.P., et al. (2007) Restoration of Shallow Lakes by Nutrient Control and Biomanipulation—The Successful Strategy Varies with Lake Size and Climate. Hydrobiologia, 581, 269-285. https://doi.org/10.1007/s10750-006-0507-3
[12]
Mucci, N., Dugheri, S., Bonari, A., Farioli, A., Rapisarda, V., Garzaro, G., et al. (2020) Health Risk Assessment Related to Hydrogen Peroxide Presence in the Workplace Atmosphere—Analytical Methods Evaluation for an Innovative Monitoring Protocol. InternationalJournalofOccupationalMedicineandEnvironmentalHealth, 33, 137-150. https://doi.org/10.13075/ijomeh.1896.01508
[13]
Kinley-Baird, C., Calomeni, A., Berthold, D.E., Lefler, F.W., Barbosa, M., Rodgers, J.H., et al. (2021) Laboratory-Scale Evaluation of Algaecide Effectiveness for Control of Microcystin-Producing Cyanobacteria from Lake Okeechobee, Florida (USA). EcotoxicologyandEnvironmentalSafety, 207, Article ID: 111233. https://doi.org/10.1016/j.ecoenv.2020.111233
[14]
Mortimer, C.H. (1941) The Exchange of Dissolved Substances between Mud and Water in Lakes. TheJournalofEcology, 29, 280-329. https://doi.org/10.2307/2256395
[15]
Lürling, M., Smolders, A.J.P. and Douglas, G.D. (2020) Methods for the Management of Internal Phosphorus Loading in Lakes. In: Steinman, A.D. and Spears, B.M., Eds., Internal Phosphorus Loading of Lakes: Causes, Case Studies, and Management, J. Ross Publishing, 77-107.
[16]
Brand, L.E., Sunda, W.G. and Guillard, R.R.L. (1986) Reduction of Marine Phytoplankton Reproduction Rates by Copper and Cadmium. JournalofExperimentalMarine Biology and Ecology, 96, 225-250. https://doi.org/10.1016/0022-0981(86)90205-4
[17]
Jančula, D. and Maršálek, B. (2011) Critical Review of Actually Available Chemical Compounds for Prevention and Management of Cyanobacterial Blooms. Chemosphere, 85, 1415-1422. https://doi.org/10.1016/j.chemosphere.2011.08.036
[18]
Barón, M., Arellano, J.B. and Gorgé, J.L. (1995) Copper and Photosystem II: A Controversial Relationship. PhysiologiaPlantarum, 94, 174-180. https://doi.org/10.1111/j.1399-3054.1995.tb00799.x
[19]
Bauzá, L., Aguilera, A., Echenique, R., Andrinolo, D. and Giannuzzi, L. (2014) Application of Hydrogen Peroxide to the Control of Eutrophic Lake Systems in Laboratory Assays. Toxins, 6, 2657-2675. https://doi.org/10.3390/toxins6092657
[20]
Lusty, M.W. and Gobler, C.J. (2020) The Efficacy of Hydrogen Peroxide in Mitigating Cyanobacterial Blooms and Altering Microbial Communities across Four Lakes in NY, Usa. Toxins, 12, Article No. 428. https://doi.org/10.3390/toxins12070428
[21]
Santos, A.A., Guedes, D.O., Barros, M.U.G., Oliveira, S., Pacheco, A.B.F., Azevedo, S.M.F.O., et al. (2021) Effect of Hydrogen Peroxide on Natural Phytoplankton and Bacterioplankton in a Drinking Water Reservoir: Mesocosm-Scale Study. WaterResearch, 197, Article ID: 117069. https://doi.org/10.1016/j.watres.2021.117069
[22]
Chen, Y., Zaman, F., Jia, Y., Huang, Y., Li, T., Bai, F., et al. (2024) Harmful Cyanobacterial Bloom Control with Hydrogen Peroxide: Mechanism, Affecting Factors, Development, and Prospects. CurrentPollutionReports, 10, 566-579. https://doi.org/10.1007/s40726-024-00328-4
[23]
Barrington, D.J., Reichwaldt, E.S. and Ghadouani, A. (2013) The Use of Hydrogen Peroxide to Remove Cyanobacteria and Microcystins from Waste Stabilization Ponds and Hypereutrophic Systems. EcologicalEngineering, 50, 86-94. https://doi.org/10.1016/j.ecoleng.2012.04.024
[24]
Vesper, S., Sienkiewicz, N., Struewing, I., Linz, D. and Lu, J. (2022) Prophylactic Addition of Glucose Suppresses Cyanobacterial Abundance in Lake Water. Life, 12, Article No. 385. https://doi.org/10.3390/life12030385
[25]
Linz, D., Struewing, I., Sienkiewicz, N., Steinman, A.D., Partridge, C.G., McIntosh, K., et al. (2024) Periodic Addition of Glucose Suppressed Cyanobacterial Abundance in Additive Lake Water Samples during the Entire Bloom Season. JournalofWaterResourceandProtection, 16, 140-155. https://doi.org/10.4236/jwarp.2024.162009
[26]
Linz, D., Partridge, C.G., Hassett, M.C., Sienkiewicz, N., Tyrrell, K., Henderson, A., et al. (2024) Changes in Cyanobacterial Phytoplankton Communities in Lake-Water Mesocosms Treated with Either Glucose or Hydrogen Peroxide. Microorganisms, 12, Article No. 1925. https://doi.org/10.3390/microorganisms12091925
[27]
Cantonati, M. and Lowe, R.L. (2014) Lake Benthic Algae: Toward an Understanding of Their Ecology. FreshwaterScience, 33, 475-486. https://doi.org/10.1086/676140
[28]
DeNicola, D.M. and Kelly, M. (2014) Role of Periphyton in Ecological Assessment of Lakes. FreshwaterScience, 33, 619-638. https://doi.org/10.1086/676117
[29]
Feminella, J.W. and Hawkins, C.P. (1995) Interactions between Stream Herbivores and Periphyton: A Quantitative Analysis of Past Experiments. JournaloftheNorthAmericanBenthologicalSociety, 14, 465-509. https://doi.org/10.2307/1467536
[30]
Tonkin, J.D., Death, R.G. and Barquín, J. (2014) Periphyton Control on Stream Invertebrate Diversity: Is Periphyton Architecture More Important than Biomass? MarineandFreshwaterResearch, 65, 818-829. https://doi.org/10.1071/mf13271
[31]
Dodds, W.K. (2003) The Role of Periphyton in Phosphorus Retention in Shallow Freshwater Aquatic Systems. JournalofPhycology, 39, 840-849. https://doi.org/10.1046/j.1529-8817.2003.02081.x
[32]
Larned, S.T., Nikora, V.I. and Biggs, B.J.F. (2004) Mass‐Transfer‐Limited Nitrogen and Phosphorus Uptake by Stream Periphyton: A Conceptual Model and Experimental Evidence. LimnologyandOceanography, 49, 1992-2000. https://doi.org/10.4319/lo.2004.49.6.1992
[33]
Pećić, M., Grašić, S., Gajić, D., Popović, S., Subakov Simić, G. and Predojević, D. (2023) Periphyton Efficiency in Phosphorus Accumulation Affected by Phytoplankton Dynamics in Reservoir for Water Supply. EcologicalEngineering, 191, Article ID: 106963. https://doi.org/10.1016/j.ecoleng.2023.106963
[34]
Liboriussen, L. and Jeppesen, E. (2005) Structure, Biomass, Production and Depth Distribution of Periphyton on Artificial Substratum in Shallow Lakes with Contrasting Nutrient Concentrations. FreshwaterBiology, 51, 95-109. https://doi.org/10.1111/j.1365-2427.2005.01481.x
[35]
Struewing, I., Sienkiewicz, N., Zhang, C., Dugan, N. and Lu, J. (2022) Effective Early Treatment of Microcystis Exponential Growth and Microcystin Production with Hydrogen Peroxide and Hydroxyapatite. Toxins, 15, Article No. 3. https://doi.org/10.3390/toxins15010003
[36]
APHA (American Public Health Association) (1999) Standard Methods for the Ex-amination of Water and Wastewater. 19th Edition, American Public Health Association.
[37]
Steinman, A.D., Lamberti, G.A., Leavitt, P.R. and Uzarski, D.G. (2017) Biomass and Pigments of Benthic Algae. In: Hauer, F.R. and Lamberti, G.A., Eds., MethodsinStreamEcology, Volume 1, Elsevier, 223-241. https://doi.org/10.1016/b978-0-12-416558-8.00012-3
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2012) The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. NucleicAcidsResearch, 41, D590-D596. https://doi.org/10.1093/nar/gks1219
[40]
Lefler, F.W., Berthold, D.E. and Laughinghouse IV, H.D. (2023) Cyanoseq: A Database of Cyanobacterial 16S rRNA Gene Sequences with Curated Taxonomy. Journal of Phycology, 59, 470-480. https://doi.org/10.1111/jpy.13335
[41]
Davis, N.M., Proctor, D., Holmes, S.P., Relman, D.A. and Callahan, B.J. (2018) Simple Statistical Identification and Removal of Contaminant Sequences in Marker-Gene and Meta-Genomics Data.
[42]
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/
[43]
Balaji-Prasath, B., Wang, Y., Su, Y.P., Hamilton, D.P., Lin, H., Zheng, L., et al. (2022) Methods to Control Harmful Algal Blooms: A Review. EnvironmentalChemistryLetters, 20, 3133-3152. https://doi.org/10.1007/s10311-022-01457-2
[44]
Pal, M., Yesankar, P.J., Dwivedi, A. and Qureshi, A. (2020) Biotic Control of Harmful Algal Blooms (HABs): A Brief Review. JournalofEnvironmentalManagement, 268, Article ID: 110687. https://doi.org/10.1016/j.jenvman.2020.110687
[45]
Zámocký, M., Gasselhuber, B., Furtmüller, P.G. and Obinger, C. (2012) Molecular Evolution of Hydrogen Peroxide Degrading Enzymes. ArchivesofBiochemistryandBiophysics, 525, 131-144. https://doi.org/10.1016/j.abb.2012.01.017
[46]
Lusty, M.W. and Gobler, C.J. (2023) Repeated Hydrogen Peroxide Dosing Briefly Reduces Cyanobacterial Blooms and Microcystin While Increasing Fecal Bacteria Indicators in a Eutrophic Pond. JournalofEnvironmentalSciences, 124, 522-543. https://doi.org/10.1016/j.jes.2021.11.031
[47]
Gao, L., Pan, X., Zhang, D., Mu, S., Lee, D. and Halik, U. (2015) Extracellular Polymeric Substances Buffer against the Biocidal Effect of H2O2 on the Bloom-Forming Cyanobacterium Microcystis Aeruginosa. WaterResearch, 69, 51-58. https://doi.org/10.1016/j.watres.2014.10.060
[48]
Gao, X., Zheng, T., Yuan, X., Dong, Y. and Liu, C. (2023) Biocidal H2O2 Treatment Emphasizes the Crucial Role of Cyanobacterial Extracellular Polysaccharides against External Strong Oxidative Stress. EnvironmentalScienceandPollutionResearch, 30, 60654-60662. https://doi.org/10.1007/s11356-023-26840-6
[49]
Drake, W.M., Scott, J.T., Evans-White, M., Haggard, B., Sharpley, A., Rogers, C.W., et al. (2011) The Effect of Periphyton Stoichiometry and Light on Biological Phosphorus Immobilization and Release in Streams. Limnology, 13, 97-106. https://doi.org/10.1007/s10201-011-0359-z
[50]
Pladdies, T., Babenzien, H. and Cypionka, H. (2004) Distribution of Nevskiaramosa and Other Rosette-Forming Neustonic Bacteria. MicrobialEcology, 47, 218-223. https://doi.org/10.1007/s00248-003-1070-3
[51]
Stürmeyer, H., Overmann, J., Babenzien, H. and Cypionka, H. (1998) Ecophysiological and Phylogenetic Studies of Nevskiaramosa in Pure Culture. AppliedandEnvironmentalMicrobiology, 64, 1890-1894. https://doi.org/10.1128/aem.64.5.1890-1894.1998
[52]
Le, V.V., Ko, S., Lee, S., Kang, M., Oh, H. and Ahn, C. (2022) Caenimonasaquaedulcis sp. nov., Isolated from Freshwater of Daechung Reservoir during Microcystis Bloom. JournalofMicrobiologyandBiotechnology, 32, 575-581. https://doi.org/10.4014/jmb.2201.01023
[53]
Vasilyeva, L.V., Omelchenko, M.V., Berestovskaya, Y.Y., Lysenko, A.M., Abraham, W., Dedysh, S.N., et al. (2006) Asticcacaulisbenevestitus sp. nov., a Psychrotolerant, Dimorphic, Prosthecate Bacterium from Tundra Wetland Soil. InternationalJournalofSystematicandEvolutionaryMicrobiology, 56, 2083-2088. https://doi.org/10.1099/ijs.0.64122-0
[54]
Glaeser, S.P. and Kämpfer, P. (2014) The Family Sphingomonadaceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E. and Thompson, F., Eds., TheProkaryotes, Springer.
[55]
Jogler, M., Chen, H., Simon, J., Rohde, M., Busse, H., Klenk, H., et al. (2013) Description of Sphingorhabdusplanktonica gen. nov., sp. nov. and Reclassification of Three Related Members of the Genus Sphingopyxis in the Genus Sphingorhabdus Gen. Nov. InternationalJournalofSystematicandEvolutionaryMicrobiology, 63, 1342-1349. https://doi.org/10.1099/ijs.0.043133-0
[56]
Nold, S.C. and Zwart, G. (1998) Patterns and Governing Forces in Aquatic Microbial Communities. AquaticEcology, 32, 17-35. https://doi.org/10.1023/a:1009991918036
[57]
Stroud, J.T., Delory, B.M., Barnes, E.M., Chase, J.M., De Meester, L., Dieskau, J., et al. (2024) Priority Effects Transcend Scales and Disciplines in Biology. TrendsinEcology&Evolution, 39, 677-688. https://doi.org/10.1016/j.tree.2024.02.004
[58]
Sand‐Jensen, K. and Søndergaard, M. (1981) Phytoplankton and Epiphyte Development and Their Shading Effect on Submerged Macrophytes in Lakes of Different Nutrient Status. Internationale Revue der Gesamten Hydrobiologie und Hydrographie, 66, 529-552. https://doi.org/10.1002/iroh.19810660406
[59]
Vadeboncoeur, Y., Vander Zanden, M.J. and Lodge, D.M. (2002) Putting the Lake Back Together: Reintegrating Benthic Pathways into Lake Food Web Models. BioScience, 52, 44-54. https://doi.org/10.1641/0006-3568(2002)052[0044:ptlbtr]2.0.co;2
[60]
Lamberti, G.A. (1996) The Role of Periphyton in Benthic Food Webs. In: Jan Stevenson, R., et al., Eds., AlgalEcology, Elsevier, 533-572. https://doi.org/10.1016/b978-012668450-6/50046-1