High temperature favors elimination of toxin-producing Microcystis and degradation of microcystins by mixotrophic Ochromonas

Chemosphere

Volumn 172, Issue , 2017, Pages 96-102

  Zhang, Lu ^a   Gu, Lei ^a   Wei, Qian ^a   Zhu, Xuexia ^a   Wang, Jun ^a   Wang, Xiaojun ^a   Yang, Zhou ^a  

^a NANJING NORMAL UNIVERSITY   (China)

Author keywords

Degradation; Microcystins; Microcystis; Ochromonas; Temperature

Indexed keywords

CHEMISTRY; DEGRADATION; TEMPERATURE;

CLEARANCE RATES; EXTRACELLULAR; HIGH TEMPERATURE; INCREASED TEMPERATURE; MICROCYSTINS; MICROCYSTIS; OCHROMONAS; REDUCTION RATIOS;

ATMOSPHERIC CHEMISTRY;

MICROCYSTIN;

ABUNDANCE; BACTERIUM; BIODEGRADATION; DEGRADATION; FLAGELLATE; GROWTH RATE; HIGH TEMPERATURE; MIXOTROPHY; TEMPERATURE EFFECT; TOXIN;

ARTICLE; BACTERIAL STRAIN; CLEARANCE; CONTROLLED STUDY; DEGRADATION; HIGH TEMPERATURE; MICROCYSTIS; MICROCYSTIS AERUGINOSA; MIXOTROPH; NONHUMAN; OCHROMONAS; PHYLOGENY; WARMING; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; THEORETICAL MODEL;

MASTIGOPHORA (FLAGELLATES); MICROCYSTIS; OCHROMONAS;

HOT TEMPERATURE; MICROCYSTINS; MICROCYSTIS; MODELS, THEORETICAL; OCHROMONAS;

EID: 85008199634     PISSN: 00456535     EISSN: 18791298     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2016.12.146     Document Type: Article

References (48)

1. Aberle, N., Bauer, B., Lewandowska, A., Gaedke, U., Sommer, U., Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production. Mar. Biol. 11 (2012), 2441–2453.
2. Allen, A.P., Gillooly, J.F., Brown, J.H., Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19 (2005), 202–213.
3. Beversdorf, L.J., Miller, T.R., Mcmahon, K.D., The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake. Plos One, 8, 2013 142-142.
4. Carmichael, W.W., Azevedo, S.M., An, J.S., Molica, R.J., Jochimsen, E.M., Lau, S., Rinehart, K.L., Shaw, G.R., Eaglesham, G.K., Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environ. Health Persp. 109 (2001), 663–668.
5. Caron, D.A., Goldman, J.C., Dennett, M.R., Effect of temperature on growth, respiration, and nutrient regeneration by an omnivorous microflagellate. Appl. Environ. Microb. 52 (1986), 1340–1347.
6. Caron, D.A., Worden, A.Z., Countway, P.D., Demir, E., Heidelberg, K.B., Protists are microbes too: a perspective. ISME J. 3 (2009), 4–12.
7. Chang, J., Chen, Z.L., Wang, Z., Shen, J.M., Chen, Q., Kang, J., Yang, L., Liu, X.W., Nie, C.X., Ozonation degradation of microcystin-LR in aqueous solution: intermediates, byproducts and pathways. Water Res. 63 (2014), 52–61.
8. Chen, M., Chen, F.Z., Yu, Y., Ji, J., Kong, F.X., Genetic diversity of eukaryotic microorganisms in Lake Taihu, a large shallow subtrophic lake in China. Microb. Ecol. 56 (2008), 572–583.
9. Chen, M., Chen, F.Z., Peng, X., Li, H., Wu, Q.L., Microbial eukaryotic community in response to Microcystis, spp. bloom, as assessed by an enclosure experiment in Lake Taihu, China. FEMS Microbiol. Ecol. 74 (2010), 19–31.
10. Clarke, A., Fraser, K.P.P., Why does metabolism scale with temperature?. Funct. Ecol. 18 (2004), 243–251.
11. Davis, T.W., Berry, D.L., Boyer, G.L., Gobler, C., The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis, during cyanobacteria blooms. Harmful Algae 8 (2009), 715–725.
12. Deng, J., Qin, B., Paerl, H.W., Zhang, Y., Ma, J., Chen, Y., Earlier and warmer springs increase cyanobacterial (Microcystis, spp.) blooms in subtropical Lake Taihu, China. Freshw. Biol. 59 (2014), 1076–1085.
13. Edwards, C., Graham, D., Fowler, N., Lawton, L.A., Biodegradation of microcystins and nodularin in freshwaters. Chemosphere 73 (2008), 1315–1321.
14. Fahnenstiel, G.L., Millie, D.F., Dyble, J., Litaker, R.W., Tester, P.A., McCormick, M.J., Rediske, R., Klarer, D., Microcystin concentrations and cell quotas in Saginaw bay, lake huron. Aquat. Ecosyst. Health 11 (2008), 190–195.
15. Fang, Y., Zhang, Y., Ma, W., Johnson, D.M., Huang, Y.P., Degradation of microcystin-LR in water: hydrolysis of peptide bonds catalyzed by maghemite under visible light. Appl. Catal. B-Environ. 160/161 (2014), 597–605.
16. Ferrão-Filho, A.S., Kozlowsky-Suzuki, B., Cyanotoxins: bioaccumulation and effects on aquatic animals. Mar. Drugs 9 (2011), 2729–2772.
17. Gan, N., Xiao, Y., Zhu, L., Wu, Z.X., Liu, J., Hu, C.L., Song, L.R., The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ. Microbiol. 14 (2012), 730–742.
18. Heinbokel, J.F., Studies on the functional role of tintinnids in the Southern California Bight. II. Grazing rates of field populations. Mar. Biol. 47 (1978), 191–197.
19. Heinze, A.W., Truesdale, C.L., Devaul, S.B., Swinden, J., Sanders, R.W., Role of temperature in growth, feeding, and vertical distribution of the mixotrophic chrysophyte Dinobryon. Aquat. Microb. Ecol. 71 (2013), 155–163.
20. Jöhnk, K.D., Huisman, J.E.F., Sharples, J., Sommeijer, B., Visser, P.M., Stroom, J.M., Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14 (2008), 495–512.
21. Jones, G.J., Orr, P.T., Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Res. 28 (1994), 871–876.
22. Joung, S.H., Oh, H.M., Ko, S.R., Ahn, C.Y., Correlations between environmental factors and toxic and non-toxic Microcystis, dynamics during bloom in Daechung reservoir, Korea. Harmful Algae 10 (2011), 188–193.
23. Keating, K.I., Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196 (1977), 885–887.
24. Kratina, P., Greig, H.S., Thompson, P.L., Carvalho-Pereira, T.S.A., Shurin, J.B., Warming modifies trophic cascades and eutrophication in experimental freshwater communities. Ecology 93 (2012), 1421–1430.
25. Lara, E., Berney, C., Ekelund, F., Harms, H., Chatzinotas, A., Molecular comparison of cultivable protozoa from a pristine and a polycyclic aromatic hydrocarbon polluted site. Soil Biol. Biochem. 39 (2007), 139–148.
26. Li, J., Shimizu, K., Maseda, H., Lu, Z., Utsumi, M., Zhang, Z., Sugiura, N., Investigations into the biodegradation of microcystin-LR mediated by the biofilm in wintertime from a biological treatment facility in a drinking-water treatment plant. Bioresour. Technol. 106 (2012), 27–35.
27. Li, D., Yu, Y., Yang, Z., Kong, F., Zhang, T., Tang, S., The dynamics of toxic and nontoxic Microcystis during bloom in the large shallow lake, Lake Taihu, China. Environ. Monit. Assess. 186 (2014), 3053–3062.
28. Mohamed, Z.A., Al-Shehri, A.M., Grazing on Microcystis aeruginosa and degradation of microcystins by the heterotrophic flagellate Diphylleia Rotans. Ecotoxicol. Environ. Safe 96 (2013), 48–52.
29. Montagnes, D.J.S., Morgan, G., Bissinger, J.E., Atkinson, D., Weisse, T., Short-term temperature change may impact freshwater carbon flux: a microbial perspective. Glob. Change Biol. 14 (2008), 2823–2838.
30. Ou, D., Song, L., Gan, N., Chen, W., Effects of microcystins on and toxin degradation by Poterioochromonas sp. Environ. Toxicol. 20 (2005), 373–380.
31. Paerl, H.W., Valdes, L.M., Joyner, A.R., Piehler, M.F., Lebo, M.E., Solving problems resulting from solutions: evolution of a dual nutrient management strategy for the eutrophying Neuse River Estuary, North Carolina. Environ. Sci. Technol. 38 (2004), 3068–3073.
32. Petchey, O.L., Mcphearson, P.T., Casey-Amp, T.M., Morin, P.J., Environmental warming alters food-web structure and ecosystem function. Nature 402 (1999), 69–72.
33. Rajasekhar, P., Fan, L., Nguyen, T., Roddick, F.A., A review of the use of sonication to control cyanobacterial blooms. Water Res. 46 (2012), 4319–4329.
34. Rigosi, A., Carey, C.C., Ibelings, B.W., Brookes, J.D., The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa. Limnol. Oceanogr 59 (2014), 99–114.
35. Robarts, R.D., Zohary, T., Temperature effects on photosynthetic capacity, respiration and growth rate of bloom-forming cyanobacteria. New Zeal. J. Mar. Fresh 21 (1987), 391–399.
36. Rose, J.M., Caron, D.A., Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol. Oceanogr. 52 (2007), 886–895.
37. Saito, T., Sugiura, N., Itayama, T., Inamori, Y., Matsumura, M., Biodegradation of Microcystis and microcystins by indigenous nanoflagellates on biofilm in a practical treatment facility. Environ. Technol. 24 (2003), 143–151.
38. Savage, V.M., Gillooly, J.F., Brown, J.G., West, G.B., Charnov, E.L., Effects of body size and temperature on population growth. Am. Nat. 163 (2004), 429–441.
39. Shi, K., Zhang, Y., Xu, H., Zhu, G., Qin, B., Huang, C., Liu, X., Zhou, Y., Lv, H., Long-term satellite observations of microcystin concentrations in Lake Taihu during cyanobacterial bloom periods. Environ. Sci. Technol. 49 (2015), 6448–6456.
40. Stanier, R.Y., Kunisawa, R., Mandel, M., Cohen-Bazire, G., Purification and properties of unicellular blue-green algae (Order Chroococcales). Bacteriol. Rev. 35 (1971), 171–205.
41. Sugiura, N., Inamori, Y., Sudo, R., Ouchiyama, T., Miyoshi, Y., Degradation of blue green alga, Microcystis aeruginosa by flagellate, Monas guttula. Environ. Technol. 11 (1990), 739–746.
42. Suikkanen, S., Fistarol, G.O., Granéli, E., Allelopathic effects of the baltic cyanobacteria Nodularia spumdigena, Aphanizomenon flos-aquae, and Anabaena lemmermannii, on algal monocultures. J. Exp. Mar. Biol. Ecol. 308 (2013), 85–101.
43. Timmermann, K., Norkko, J., Janas, U., Norkko, A., Bo, G.G., Bonsdorff, E., Modelling macrofaunal biomass in relation to hypoxia and nutrient loading. J. Mar. Syst. 105/108 (2012), 60–69.
44. Wilken, S., Wiezer, S., Huisman, J., Donk, E.V., Microcystins do not provide anti-herbivore defence against mixotrophic flagellates. Aquat. Microb. Ecol. 59 (2010), 207–216.
45. Wilken, S., Huisman, J., Naus-Wiezer, S.M.H., Van Donk, E., Mixotrophic organisms become more heterotrophic with rising temperature. Ecol. Lett. 16 (2013), 225–233.
46. Wu, T., Qin, B., Zhu, G., Luo, L., Ding, Y., Bian, G., Dynamics of cyanobacterial bloom formation during short-term hydrodynamic fluctuation in a large shallow, eutrophic, and wind-exposed Lake Taihu, China. Environ. Sci. Pollut. Res. 20 (2013), 8546–8556.
47. Yang, Z., Zhang, L., Zhu, X.X., Wang, J., Montagnes, D.J.S., An evidence-based framework for predicting the impact of differing autotroph-heterotroph thermal sensitivities on consumer–prey dynamics. ISME J. 10 (2016), 1767–1778.
48. Zhang, X., Hu, H., Men, Y., Christoffersen, K.S., The effect of Poterioochromonas abundance on production of intra- and extracellular microcystin-LR concentration. Hydrobiologia 652 (2010), 237–246.