Abstract
Microorganisms such as bacteria are considered to be control agents against toxic cyanobacterial blooms such as Microcystis aeruginosa. We investigated cyanobactericidal bacteria and growth-inhibiting bacteria against M. aeruginosa in the biofilm on the surface of the water plants Trapa japonica, Myriophyllum verticallatum and Utricularia vulgaris at three sites in Ohnuma Quasi-National Park during the period from July to October 2012. Bacteria were isolated using nutrient agar plates, and killing abilities and growth-inhibiting abilities of isolated bacteria were examined for M. aeruginosa with co-culture experiments. Effective bacteria (sums of cyanobactericidal bacteria and growth-inhibiting bacteria) were confirmed from the leaves and water roots of T. japonica with densities of 3.6 × 105 CFU g−1 wet weight—1.2 × 107 CFU g−1 wet weight and 1.5 × 106 CFU g−1 wet weight—1.4 × 108 CFU g−1 wet weight, respectively. M. verticillatum and U. vulgaris harbored effective bacteria with densities of 2.5 × 106 CFU g−1 wet weight—1.1 × 107 CFU g−1 wet weight and 2.3 × 106 CFU g−1 wet weight—9.2 × 106 CFU g−1 wet weight, respectively. Effective bacteria were also detected from water samples collected from all three sites and the most numerous values were detected at Sansui with abundant water plants such as T. japonica and M. verticillatum. Densities of M. aeruginosa tended to be fewer at Sansui and were more abundant at Ohnuma Park with almost no water plants. The results of PCA suggested that the absence and/or lower densities of M. aeruginosa was closely related to the abundant presence of effective bacteria detected from the water and biofilms of water plants such as T. japonica at Sansui. The present findings provide new insights on the ecology of cyanobactericidal bacteria and growth-inhibiting bacteria, and suggest that water plants provide an environment that influences the abundance of cyanobacterial blooms in freshwater ecosystems.
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References
Akiyama M, Kunii H (1989) Allelopathic effects of aquatic seed plants on algal plankton. Bull Water Plant Soc Jpn 37:11–16 (in Japanese)
Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann Rev Mar Sci 4:143–176
Carmichael WW, Jones CLA, Mahmood NA, Thesis WC, Krogh P (1985) Algal toxins and water-based disease. CPC Crit Rev Environ Control 15:275–283
Codd GA (2000) Cyanobacterial toxins, the perception of water quality and the prioritization of eutrophication control. Ecol Eng 16:51–60
Cronberg G, Annadotter H (2006) Manual on aquatic cyanobacteria: a photo guide and a synopsis of their toxicology. ISSHA and IOC-UNESCO, Copenhagen, p 106
Daft MJ, McCord SB, Stewart WDP (1975) Ecological studies on algal-lysing bacteria in fresh waters. Freshw Biol 5:577–596
Herry SE, Fathalli A, Rejeb AJ, Bouaïcha N (2007) Seasonal occurrence and toxicity of Microcystis spp. and Oscillatoria tenuis in the Lebna Dam, Tunisia. Water Res 42:1263–1273
Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilize clear-water states in shallow lakes? Basic Appl Ecol 9:422–432
Iamchaturapatr J, Yi WS, Rhee JS (2007) Nutrient removals by 21 aquatic plants for vertical free surface-flow (VFS) constructed wetland. Ecol Eng 29:287–293
Imai I (2010) Ecology and physiology of anti-Microcystis bacteria in reed (Phragmites australis) communities. IFO Res Commun 24:201–212
Imai I (2015) Interactions between harmful algae and algicidal and growth-inhibiting bacteria associated with seaweeds and seagrasses. In: Ohtsuka S, Suzaki T, Horiguchi T, Suzuki N, Not F (eds) Marine protists: diversity and dynamics. Springer, Tokyo, pp 597–619
Imai I, Fujimaru D, Nishigaki T (2002) Co-culture of fish with macroalgae and associated bacteria: a possible mitigation strategy for noxious red tides in enclosed coastal sea. Fish Sci 68(Suppl):493–496
Imai I, Kido T, Yoshinaga I, Ohgi K, Nagai S (2013) Isolation of Microcystis-killer bacterium Agrobacterium vitis from the biofilm on the surface of the water plant Egeria densa. In: Pagou P, Hallegraeff G (eds) Proceedings of the 14th international conference of harmful algae, ISSHA & IOC-UNESCO, pp 150–152
Imai I, Ohgi K, Mizuhara S, Yamaguchi A, Kaeriyama M (2014) Control of Microcystis aeruginosa blooms by using microorganisms in waters from reed community and water plant bed. In: Kim HG, Reguera B, Hallegraeff GM, Lee CK, Han MS, Choi JK (eds) Proceedings of the 15th international conference of harmful algae, ISSHA and IOC-UNESCO, pp 184–187
Imai I, Yamamoto T, Ishii K, Inaba N, Yamamoto K (2016) Prevention of harmful algal blooms by algicidal bacteria associated with eelgrasses. J Water Waste 58:295–300
Inaba N, Trainer VL, Onishi Y, Ishii KI, Wyllie-Echeverria S, Imai I (2017) Algicidal and growth-inhibiting bacteria associated with seagrass and macroalgae beds in Puget Sound, WA, USA. Harmful Algae 62:136–147
Ishida Y, Shibata K, Uchida H, Kadota H (1986) Distribution of obligately oligotrophic bacteria in Lake Biwa. Bull Jpn Soc Sci Fish 46:1151–1158
Kojima S, Miyashita Y, Hagiwara T, Yamaguchi A, Imai I (2016) Possible control strategy of cyanobacterial blooms by bacteria from reed (Phragmites australis) communities in lakes of Ohnuma Quasi-National Park, Hokkaido. Bull Fish Sci Hokkaido Univ 66:19–28
Lurling M, van Geest G, Sheffer M (2006) Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes, Chara, Elodea and Myriophyllum. Hydrobiologia 556:209–220
Manage PM, Kawabata Z, Nakano S (2000) Algicidal effects of the bacterium Alcaligenes denitrificans on Microcystis spp. Aquat Microb Ecol 22:111–117
Manage PM, Kawabata Z, Nakano S (2001) Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2:73–78
Miyashita Y, Junki K, Kuniaki T, Imai I (2015) Water purification by the water plant Trapa japonica artificially seeded in a detention pond at Karima River area in Hokkaido. Bull Fish Sci Hokkaido Univ 65:101–109
Nakai S, Yutaka I, Masaaki H, Murakami A (1997) Growth-inhibition of blue-green algae by allelopathic effects of macrophytes. Water Treat Biol 33:215–222
Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Tot Environ 409:1739–1745
Park JH, Yoshinaga I, Nishikawa T, Imai I (2010) Algicidal bacteria in particle-associated form and in free-living form during a diatom bloom in the Seto Inland Sea. Jpn Aquat Microb Ecol 60:151–161
Ruggiero A, Solimini AG, Carchini G (2003) Nutrient and chlorophyll a temporal patterns in eutrophic mountain ponds with contrasting macrophyte coverage. Hydrobiologia 506–509:657–663
Sakami T, Sakamoto S, Takagi S, Inaba N, Imai I (2017) Distribution of three algicidal Alteromonas sp. strains in seagrass beds and surrounding areas in the Seto Inland Sea, Japan. Fish Sci 83:113–121
Shimizu T, Oda T, Ito H, Imai I (2017) Isolation and characterization of algicidal bacteria and its effect on a musty odor-producing cyanobacterium Dolichospermum crassum in reservoir. Water Sci Technol Water Supply 17:792–798
Takahashi K, Amano Y, Machida M (2012) Growth and competitive characteristics of the blue-green alga Microcystis aeruginosa and the diatom Cyclotella sp. under nitrogen limitation. Jpn J Phycol (Sôrui) 60:1–8
Takamura N, Kadono Y, Fukushima M, Nakagawa M, Kim B-HO (2003) Effects of aquatic macrophytes on water quality and phytoplankton communities in shallow lakes. Ecol Res 18:381–395
van Donk E, van de Bund WJ (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72:261–274
Watanabe M, Ichimura T (1977) Fresh- and salt-water forms of Spirulina platensis in axenic cultures. Bull Jpn Soc Phycol 25(Suppl):371–377 (Mem Iss Yamada)
Yagi O, Hagiwara T, Takamura Y, Sudo R (1984) Growth characteristics of axenic and unialgal Microcystis isolated from Lake Kasumigaura. Jpn J Wat Pollut Res 7:496–503
Yanagi T (2008) “Sato-umi”—a new concept for sustainable fisheries. In: Tsukamoto K, Kawamura T, Takeuchi T, Beard TD Jr (eds) Fisheries for global welfare and environment. TERRAPUB, Tokyo, pp 351–358
Yang F, Li X, Li Y, Wei H, Yu G, Yin L, Liang G, Pu Y (2013) Lysing activity of an indigenous algicidal bacterium Aeromonas sp. against Microcystis spp. isolated from Lake Taihu. Environ Technol 34:1421–1427
Acknowledgements
We would like to express our sincere gratitude to Professor Kuniaki Tanaka of the Environmental Science Course, Hokkaido University of Education, Hakodate Campus for helpful advice during this research. We express our sincere thanks to those at Ohnuma Boating Co., Ltd. for overall cooperation with this research. We are grateful to Mr. Tsukasa Miyazaki of Ohnuma Fisheries Cooperative Association for his helpful information on Lake Ohnuma. We appreciate Messrs. Keigo Sekiguchi, Taku Kosugi and Akira Kobayashi of Nanae Town Office for their diligent cooperation with this study.
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Miyashita, Y., Hagiwara, T. & Imai, I. The existence of cyanobactericidal bacteria and growth-inhibiting bacteria on water plants in Lake Ohnuma, Japan. Limnology 20, 39–53 (2019). https://doi.org/10.1007/s10201-018-0542-6
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DOI: https://doi.org/10.1007/s10201-018-0542-6