Effect of two co-habitat bacteria on the recruitment of dormant Microcystis aeruginosa cells

ZOU Wan-sheng; Mo Ping; WANG Zhi; LIU Liang-guo

PDF(1570 KB)

China Environmental Science ›› 2024, Vol. 44 ›› Issue (8) : 4366-4379.

Water Pollution Control

Effect of two co-habitat bacteria on the recruitment of dormant Microcystis aeruginosa cells

ZOU Wan-sheng¹, Mo Ping¹, WANG Zhi², LIU Liang-guo¹

Author information +

History +

Abstract

Both benthic bacteria and dormant M. aeruginosa cells (DMCs) are important members of aquatic ecosystems. In our previous research work, one strain of algae-inhibiting bacterium (Sphingobacterium kitahiroshimense 10C^T, strain H1) and one strain of algae-promoting bacterium (Bacillus zhangzhouensis DW5-4^T, strain H2) were isolated simultaneously from the same aquaculture fishpond. Recruitment experiments were conducted to unveil the combined impact of the two bacteria on the DMCs recruitment. Strain H1 and H2 at different bacterial ratios were mixed with DMCs and embedded into sediments. The experiments were conducted at temperature 15°C and 25°C, a photoperiod of 12h light: 12h dark, and a light intensity of 15μmol/(m²·s) for 21 d. The results showed that when the bacterial ratio was less than three, the concentration of soluble extracellular polysaccharides (SPS) of DMCs in bacterial groups significantly reduced compared with the control group (sterile group), while there was no significant difference in capsular extracellular polysaccharides (CPS) and photosynthetic efficiency (Fv/Fm) of DMCs (P>0.05). The SPS concentration decrease did not affect Fv/Fm, and the strains H1 and H2 significantly improved the recruitment rate of DMCs by secreting three metabolites. When the bacterial ratio was greater than five, the SPS, CPS, and Fv/Fm in the bacterial groups were significantly lower compared with the control group (P<0.05). The decrease of CPS concentration inhibited the photosynthetic efficiency (Fv/Fm) of DMCs, and under high bacterial ratio condition the strains H1 and H2 synergistically reduced the recruitment rate of DMCs by reducing the photosynthetic efficiency (Fv/Fm) of DMCs and secreting two metabolites that effectively inhibited DMCs recruitment (the recruitment rate of DMCs under pure metabolite was higher than that of the bacterial groups). Interestingly, field qualitative experiments confirmed that the different bacterial ratio of strains H1 and H2 significantly affects the recruitment rate of DMCs, and the experimental results provide new ideas for predicting the recruitment rate of DMCs in early spring and a new approach for early preventing formation of M. aeruginosa blooms.

Key words

Microcystis aeruginosa / antioxidant enzyme / extracellular polysaccharide / freshwater bacteria / photosynthetic efficiency

Cite this article

EndNote

Ris (Procite)

Bibtex

Download Citations

ZOU Wan-sheng, Mo Ping, WANG Zhi, LIU Liang-guo. Effect of two co-habitat bacteria on the recruitment of dormant Microcystis aeruginosa cells[J]. China Environmental Science. 2024, 44(8): 4366-4379

References

[1] Wan N, Tang J, Li Q M, et al. The responses of Microcystis to sediment environments and the assessment for its overwintering a simulation study in a novel device [J]. Fresenius Environmental Bulletin, 2008,17(12b):2146-2151.
[2] Delphine C R, Warwick F V. Characterization of phytoplankton seed banks in the sediments of a drinking water reservoir [J]. Lake and Reservoir Management, 2014,30:371-380.
[3] Borges H, Wood S A, Puddick J, et al. Intracellular, environmental and biotic interactions influence recruitment of benthic Microcystis (Cyanophyceae) in a shallow eutrophic lake [J]. Journal of Plankton Research, 2016,00:1-13.
[4] Xie L Q, Xie P, Tang H J. Enhancement of dissolved phosphorus release from sediment to lake water by Microcystis blooms-an enclosure experiment in a hyper-eutrophic, subtropical Chinese lake [J]. Environmental Pollution, 2003,122:391-199.
[5] Schone K, Jähnichen S, Ihle T. Arriving in better shape: Benthic Microcystis as inoculum for pelagic growth [J]. Harmful Algae, 2010, 9(5):494-503.
[6] Zhang J, Li C H, ChunY E. Effects of Hydrilla verticillata decomposition on recruitment of the dormant Microcystis spp [J]. Research of Environmental Sciences, 2012,25(1):43-50.
[7] Tang J, Song L R, Sun S S, et al. Recruitment ability of Microcystis aeruginosa under low light-low temperature combination [J]. Water Research, 2010,31(12):2932-2937.
[8] Misson B, Delphinelatour. Influence of light, sediment mixing, temperature and duration of the benthic life phase on the benthic recruitment of Microcystis [J]. Journal of Plankton Research, 2012, 34(2):113-119.
[9] Tan X, Kong F X, Zhang M, et al. Effects of temperature on phytoplankton recruitment and variations in phytoplankton community composition [J]. Journal of Freshwater Ecology, 2009,24:339-341.
[10] Yamamoto Y. Effect of temperature on recruitment of cyanobacteria from sediment and bloom formation in a shallow pond [J]. Plankton Benthos Research, 2009,4:95-103.
[11] Tsujimura S, Tsukada H, Nakahara H. Seasonal variations of Microcystis populations in sediments of lake Biwa Japan [J]. Hydrobiologia, 2000,434(3):183-192.
[12] Hodoki Y, Ohbayashi K, Kobayashi Y, et al. Temporal variation in cyanobacteria species composition and photosynthetic activity in experimentally induced blooms [J]. Journal of Plankton Research, 2011,33:1410-1416.
[13] Zou W S, Wang Z, Song Q S, et al. Recruitment-promoting of dormant Microcystis aeruginosa by three benthic bacterial species [J]. Harmful Algae, 2018,77:18-28.
[14] Forni C, Telo F R, Caiola G. Comparative analysis of the polysaccharides produced by different species of Microcystis (Chroococcal, Cyanophyta) [J]. Phycologia, 1997,36(3):181-185.
[15] Chen M, Tian L, Ren C, et al. Extracellular polysaccharide synthesis in a bloom-forming strain of Microcystis aeruginosa: Implications for colonization and buoyancy [J]. Scientific Report, 2019,9:1251.
[16] Brunberg A K, Lyra C, Kaarina Sivonen. High diversity of cultivable heterotropic bacteria in association with cyanobacterial water blooms [J]. ISME Journal, 2009,3:314-325.
[17] Yang C Y, Yi L, Zhou Y Y, et al. Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China [J]. Scientific Report, 2015, 5:8476-8486.
[18] Verspagen J M H, Sneldere O F, Visser P M, et al. Recruitment of benthic Microcystis (Cyanophyceae) to the water column: internal buoyancy changes or susupension [J]. Journal of Phycology, 2004,40:260-270.
[19] Berrendero E, Valiente E F, Perona E, et al. Nitrogen fixation in a non-heterocystous cyanobacterial mat from a mountain river [J]. Scientific Report, 2016,6:30920-30930.
[20] Yang Z, Kong F X, Shi X L, et al. Changes in the morphology and polysaccharide content of Microcystis aeruginosa (Cyanobacteria) during flagellate grazing [J]. Journal of Phycology, 2008,44(3):716-720.
[21] Pautova A K, Sobolev P D, Revelsky A I, et al. Analysis of phenylcarboxylic acid-type microbial metabolites by microextraction by packed sorbent from blood serum followed by GC-MS detection [J]. Clinical Mass Spectrometry, 2019,14:46-53.
[22] Wang J, Peng YD, Wang Z, et al. Transcriptional response of Microcystis aeruginosa to the recruitment promoting-benthic bacteria [J]. Journal of Oceanology and Limnology, 2022,40(1):153-162.
[23] Yamamoto Y, Kouchiwa T, Hodoki Y, et al. Distribution and identification of actinomycetes lysing cyanobacteria in a eutrophic lake [J]. Journal of Applied Phycology, 1998,10(4):391-397.
[24] Imamura N, Motoike I, Shimada N, et al. An efficient screening approach for anti-Microcystis compounds based on knowledge of aquatic microbial ecosystem [J]. Journal of Antibiotics, 2001,54(7):582.
[25] 洪桂云,马少雄,王佳,等.高效铜绿微囊藻溶藻菌WJ6的分离鉴定及溶藻特性[J]. 中国环境科学, 2018,38(11):4269-4275. HONG Gui-yun, MA Shao-xiong, WANG Jia, et al. Isolation and identification of an efficient algicidal bacteria strain and algicidal characteristics on Microcystis aeruginosa [J]. China Environmental Science, 2018,38(11):4269-4275.
[26] Arora-Williams K, Olesen S W, Scandella B P, et al. Dynamics of microbial populations mediating biogeochemical cycling in a freshwater lake [J]. Microbiome, 2018,6:165-215.
[27] 邵继海.生物源物质和溶藻菌对铜绿微囊藻抑制作用机理研究[D]. 武汉:中国科学院大学, 2010. Shao J. Inhibitory mechanisms of biological originated substancesand algicidal bacterium on the control of Microcystis aeruginosa [D]. Wuhan: University of Chinese Academy of Sciences, 2010.
[28] Li H, Barber M, Lu J, et al. Microbial community successions and their dynamic functions during harmful cyanobacterial blooms in a freshwater lake [J]. Water Research, 2020,185:116292-116304.
[29] 母锐敏,贾静静,张盛至.溶藻细菌FS1的溶藻效果与机制初探[J]. 微生物学杂志, 2015,35(6):16-20. MU Rui-min, JIA Jing-jing, ZHANG Sheng-zhi, et al. Initial Investigation on Algicidal Effect and Mechanism of Algae-lytic Bacteria FS1[J]. Journal of Microbiology, 2015,35(6):16-20
[30] Tang J, Song, L R, Sun, S S, et al. Recruitment ability of Microcystis aeruginosa under low light-low temperature combination [J]. Water Research, 2010,31(12):2932-2937.
[31] Karlson A M L, Nascimento F J A, Sanna S, et al. Benthic fauna affects recruitment from sediments of the harmful cyanobacterium Nodularia spumigena [J]. Harmful Algae, 2012,20:126-131.
[32] Misson B, Dephinelatou R. Influence of light, sediment mixing, temperature and duration of the benthic life phase on the benthic recruitment of Microcystis [J]. Journal of Plankton Research, 2012, 34(2):113-119.
[33] Neilan B A, Pearson L A, Muenchhoff J, et al. Environmental conditions that influence toxin biosynthesis in cyanobacteria [J]. Environmental Microbiology, 2013,15(5):1239-1253.
[34] Ma J R, Qin B Q, Paerl H W, et al. The persistence of cyanobacterial (Microcystis spp.) blooms throughout winter in Lake Taihu, China [J]. Limnology and Oceanography, 2016,61:711-722.
[35] Mallick N, Mohn F H. Reactive oxygen species: response of algal cells [J]. Journal of Plant Physiology, 2000,157:183-193.
[36] Suzuki N, Mittler R. Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction [J]. Physiologia Plantarum, 2010,126(1):45-51.
[37] Imlay J A. Pathways of oxidative damage [J]. Annual Review of Microbiology, 2003,57(1):395-418.
[38] Wang Y, Liu Q, Wei Z, et al. Thiazole Amides, A Novel Class of Algaecides against Freshwater Harmful Algae [J]. Scientific Reports, 2018,8(1):8555.
[39] Han P P, Shen, S G, Guo R, et al. ROS Is a Factor Regulating the Increased Polysaccharide Production by Light Quality in the Edible Cyanobacterium Nostoc flagelliforme [J]. Journal of Agricultural and Food Chemistry, 2019,67(8):2235-2244.
[40] Nakagawa M, Takamura Y, Yagi O. Isolation and characterization of the slime from a cyanobacterium,Microcystis aeruginosa K-3A [J]. Agricultural and Biological Chemistry, 1987,51(2):329-337.
[41] Shen H, Niu Y, Xie P, et al. Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria [J]. Freshwater Biology, 2011,56(6):1065-1080.
[42] Blanco Y, Alfonso Rivas L, Gonzalez-Toril E, et al. Environmental parameters, and not phylogeny, determine the composition of extracellular polymeric substances in microbial mats from extreme environments [J]. Science of the Total Environment, 2019,650(1):384-393.
[43] Li Y, Zhu H, Lei X, et al. The first evidence of deinoxanthin from Deinococcus sp. Y35with strong algicidal effect on the toxic dinoflagellate Alexandrium tamarense [J]. Journal of hazardous materials, 2015,290:87-95.
[44] Zhao L, Chen L, Yin P. Algicidal metabolites produced by Bacillus sp. strain B1against Phaeocystis globosa [J]. Journal of Industrial Microbiology & Biotechnology, 2014,41(3):593-599.
[45] Li F M, Hu H Y. Isolation and Characterization of a Novel Antialgal Allelochemical from Phragmites communis [J]. Applied & Environmental Microbiology, 2005,71(11):6545-6553.
[46] Zhang H, Hui W, Wei Z, et al. Toxic Effects of Prodigiosin Secreted by Hahella sp. KA22 on Harmful Alga Phaeocystis globosa [J]. Frontiers in Microbiology, 2017,8:999.
[47] Yu Y, Zeng Y, Li J, et al. An algicidal Streptomyces amritsarensis strain against Microcystis aeruginosa strongly inhibits microcystin synthesis simultaneously [J]. Science of The Total Environment, 2019, 650:34-43.