Abstract
Intensive and semi-intensive aquaculture systems typically produce high loads of nutrients in their discharge, potentially leading to the development and persistence of harmful algal blooms (HABs). Algicidal bacteria, which inhibit algal growth or kill algal cells, offer a promising biocontrol strategy for reducing HAB. The strain JZBC1, which displays strong algicidal activity against the HAB species Scrippsiella trochoidea, was previously isolated from a dinoflagellate bloom area and identified as Bacillus cereus. In this study, strain JZBC1 was fermented in 2 L and 50 L systems, and then, algicidal properties of JZBC1 fermentation products on the harmful dinoflagellate species S. trochoidea, Prorocentrum micans, and Peridinium umbonatum were examined. Bacterial concentrations of strain JZBC1 reached 6.23 × 109 and 4.47 × 109 CFU/mL in 2 L and 50 L cultures, respectively, and thus effectively expanded during fermentation. Strain JZBC1 showed substantial algicidal activities and a wide algicidal range toward harmful dinoflagellates. Vegetative JZBC1 cells exhibited the best inhibitory and algicidal effects in 1 day. Strain JZBC1 can be formulated into a powder, and the spores can be activated before field application to increase their efficacy. These findings will facilitate large-scale fermentation production and application of Bacillus strain JZBC1 for controlling dinoflagellate blooms in aquaculture ponds.
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Abbreviations
- HABs:
-
Harmful Algal Blooms
- CFU:
-
Colony Forming Units
References
Alonso-Rodrıguez R, Páez-Osuna F (2003) Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: a review with special reference to the situation in the Gulf of California. Aquaculture 219(1–4):317–336. https://doi.org/10.1016/S0044-8486(02)00509-4
Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25(4):704–726. https://doi.org/10.1007/BF02804901
Anderson DM, Cembella AD, Hallegraeff GM (2012) Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu Rev Mar Sci 4:143–176. https://doi.org/10.1146/annurev-marine-120308-081121
Cao YC, Wen GL, Li ZJ, Liu XZ, Hu XJ, Zhang JS, He J (2014) Effects of dominant microalgae species and bacterial quantity on shrimp production in the final culture season. J Appl Phycol 26(4):1749–1757. https://doi.org/10.1007/s10811-013-0195-0
Cao YC, Wen GL, Li ZJ, Hu XJ, Xi JY, Li SS, Huang HH (2019) Bacillus cereus strain JZBC1 dissolving dominant dinoflagellate of pond-Scrippsiella trochoidea and its application. China patent. ZL201610209371.X
Chang M, Sun QH, Zhou SH, Ni JR (2010) Factors analysis and process selection for the production of Bacillus thuringiensis based biopesticides. Ecol Environ Sci 19(6):1471–1477. https://doi.org/10.3969/j.issn.1674-5906.2010.06.038
Chrisotph P, Uwe T, Hanne G (2000) Improved secondary metabolite production in the genus Streptosporangium by optimization of the fermentation condition. J Biotechnol 80(2):135–142. https://doi.org/10.1016/S0168-1656(00)00249-2
Gárate-Lizárraga I, Band-Schmidt CJ, López-Cortés DJ, Muñetón-Gómez Mdel S (2009) Bloom of Scrippsiella trochoidea (Gonyaulacaceae) in a shrimp pond in the southwestern Gulf of California, Mexico. Mar Pollut Bull 58(1):145–149. https://doi.org/10.1016/j.marpolbul.2008.09.016
Guan C, Guo X, Cai G, Zhang H, Li Y, Zheng W, Zheng T (2014) Novel algicidal evidence of a bacterium Bacillus sp. LP-10 killing Phaeocystis globosa, a harmful algal bloom causing species. Biol Control 76:79–86. https://doi.org/10.1016/j.biocontrol.2014.05.007
Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Springer, Boston. https://doi.org/10.1007/978-1-4615-8714-9_3
Hallegraeff GM (1992) Harmful algal blooms in the Australian region. Mar Pollut Bull 25(5–8):186–190. https://doi.org/10.1016/0025-326X(92)90223-S
Hare CE, Demir E, Coyne KJ, Craig Cary SC, Kirchman DL, Hutchins DA (2005) A bacterium that inhibits the growth of Pfiesteria piscicida and other dinoflagellates. Harmful Algae 4(2):221–234. https://doi.org/10.1016/j.hal.2004.03.001
Heisler J, Glibert PM, Burkholder JM, Anderson DM, Cochlan W, Dennison WC, Dortch Q, Gobler CJ, Heil CA, Humphries E, Lewitus A, Magnien R, Marshall HG, Sellner K, Stockwell DA, Stoecker DK, Suddleson M (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8(1):3–13. https://doi.org/10.1016/j.hal.2008.08.006
Hu XJ, Wen GL, Xu WJ, Xu Y, Su HC, Yang K, Xu YN, Li ZJ, Cao YC (2019) Effects of the algicidal bacterium CZBC1 on microalgal and bacterial communities in shrimp culture. Aquacult Environ Interact 11:279–290. https://doi.org/10.3354/aei00311
Khan MR, Majid S, Mohidin FA, Khan N (2011) A new bioprocess to produce low cost powder formulations of biocontrol bacteria and fungi to control fusarial wilt and root-knot nematode of pulses. Biol Control 59(2):130–140. https://doi.org/10.1016/j.biocontrol.2011.04.007
Kim YS, Lee DS, Jeong SY, Lee WJ, Lee MS (2009) Isolation and characterization of a marine algicidal bacterium against the harmful Raphidophyceae Chattonella marina. J Microbiol 47(1):9–18. https://doi.org/10.1007/s12275-008-0141-z
Lalloo R, Maharajh D, Görgens J, Gardiner N (2010) A downstream process for production of a viable and stable Bacillus cereus aquaculture biological agent. Appl Microbiol Biotechnol 86(2):499–508. https://doi.org/10.1007/s00253-009-2294-z
Li ZH, Geng MX, Yang H (2015) Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa. Appl Microbiol Biotechnol 99(2):981–990. https://doi.org/10.1007/s00253-014-6043-6
Li SS, Cao YC, Hu XJ, Li ZJ, Xu Y, Yang Y, Xu CW, Wen GL (2017a) Optimization for cultivatioparameters of Bacillus sp. A4 using response surface methodology. South China Fish Sci 13:85–93. https://doi.org/10.3969/j.issn.2095-0780.2017.05.012
Li SS, Cao YC, Li ZJ, Hu XJ, Xu Y, Xu WJ, Yang K, Su HC, Wen GL (2017b) The effects of different carbon and nitrogen nutrients and culture conditions on the growth of Bacillus sp. strain A4. Prog Fish Sci 38:119–126. https://doi.org/10.11758/yykxjz.20160923001
Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51(2):139–144. https://doi.org/10.1111/j.1550-7408.2004.tb00538.x
Meyer N, Bigalke A, Kaulfuß A, Pohnert G (2017) Strategies and ecological roles of algicidal bacteria. FEMS Microbiol Rev 41(6):880–899. https://doi.org/10.1093/femsre/fux029
Mu RM, Fan ZQ, Pei HY, Yuan XL, Liu SX, Wang XR (2007) Isolation and algae-lysing characteristics of the algicidal bacterium B5. J Environ Sci 19(11):1336–1340. https://doi.org/10.1016/S1001-0742(07)60218-6
Pokrzywinski KL, Place AR, Warner ME, Coyne KJ (2012) Investigation of the algicidal exudate produced by Shewanella sp. IRI-160 and its effect on dinoflagellates. Harmful Algae 19:23–29. https://doi.org/10.1016/j.hal.2012.05.002
Pokrzywinski KL, Tilney CL, Modla S, Caplan JL, Ross J, Warner ME, Coyne KJ (2017) Effects of the bacterial algicide IRI-160AA on cellular morphology of harmful dinoflagellates. Harmful Algae 62:127–135. https://doi.org/10.1016/j.hal.2016.12.004
Prabakaran G, Hoti SL (2008) Optimization of spray-drying conditions for the large-scale preparation of Bacillus thuringiensis var. israelensis after downstream processing. Biotechnol Bioeng 100(1):103–107. https://doi.org/10.1002/bit.21722
Qiu J, Dong SL, Wang CY (2005) Allelopathic growth inhibition of Prorocentrum micans (Dinophyta) by Ulva pertusa and Ulva linza (Chlorophyta) in laboratory cultures. Eur J Phycol 40(1):31–37. https://doi.org/10.1080/09670260400019741
Shi SY, Liu YD, Shen YW, Li GB, Li DH (2006) Lysis of Aphanizomenon flos-aquae (Cyanobacterium) by a bacterium Bacillus cereus. Biol Control 39(3):345–351. https://doi.org/10.1016/j.biocontrol.2006.06.011
Su JQ, Yang XR, Zheng TL, Tian Y, Jiao NZ, Cai LZ, Hong HS (2007) Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense. Harmful Algae 6(6):799–810. https://doi.org/10.1016/j.hal.2007.04.004
Sun HY, Zhang Y, Chen HR, Hu CX, Li H, Hu ZL (2016) Isolation and characterization of the marine algicidal bacterium Pseudoalteromonas S1 against the harmful alga Akashiwo sanguinea. Mar Biol 163(3):66. https://doi.org/10.1007/s00227-016-2836-8
Sun R, Sun P, Zhang J, Esquivel-Elizondo S, Wu Y (2017) Microorganisms-based methods for harmful algal blooms control: a review. Bioresour Technol 248(B):12–20. https://doi.org/10.1016/j.biortech.2017.07.175
Tang YZ, Gobler CJ (2012) Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on eastern oyster (Crassostrea virginica) and northern quahog (Mercenaria mercenaria) larvae. Mar Biol 159(1):199–210. https://doi.org/10.1007/s00227-011-1800-x
Tilney CL, Pokrzywinski KL, Coyne KJ, Warner ME (2014) Growth, death, and photobiology of dinoflagellates (Dinophyceae) under bacterial-algicide control. J Appl Phycol 26(5):2117–2127. https://doi.org/10.1007/s10811-014-0248-z
Wang BX, Yang XR, Lu JL, Zhou YY, Su JQ, Tian Y, Zhang J, Wang GZ, Zheng TL (2012) A marine bacterium producing protein with algicidal activity against Alexandrium tamarense. Harmful Algae 13:83–88. https://doi.org/10.1016/j.hal.2011.10.006
Wang SL, Cao YC, Xu Y, Hu XJ, Li ZJ, Wu Y (2016) Regulation of Bacillus cereus to microalgae community in shrimp aquaculture water. South China Fish Sci 12:9–16. https://doi.org/10.3969/j.issn.2095-0780.2016.01.002
Xi JY (2016) Algicidal effects of algicidal bacteria against dinoflagellate from shrimp ponds. Shanghai Ocean University
Xi JY, Cao YC, Li ZJ, Wen GL, Xu WJ, Zheng QH, Li ZC, Xu YN (2016) Specificity of algicidal activity against four species of microalgae by algicidal bacterium A2. South China Fish Sci 12(5):34–42. https://doi.org/10.3969/j.issn.2095-0780.2016.05.005
Xu J, Wu X, Yang Y, Xu S, Kang Y, Fu X, Yue H, Shi JQ, Wu ZX (2016) Changes in growth, photosynthesis and chlorophyll fluorescence in the freshwater dinoflagellate Peridinium umbonatum (Peridiniales, Pyrrophyta) in response to different temperatures. Phycologia 55(4):469–477. https://doi.org/10.2216/PH15-148.1
Yang YY, Li ZJ, Chen YQ, Yang K, Wen GL, Ding X (2005) Fermentation technology of probiotic strain D-1. South China Fish Sci 1:44–49. https://doi.org/10.3969/j.issn.2095-0780.2005.06.007
Yang YF, Hu XJ, Zhang J, Gong YX (2013) Community level physiological study of algicidal bacteria in the phycosphere of Skeletonema costatum and Scrippsiella trochoidea. Harmful Algae 28:88–96. https://doi.org/10.1016/j.hal.2013.05.015
Yang X, Li X, Zhou Y, Zheng W, Yu C, Zheng T (2014) Novel insights into the algicidal bacterium DH77-1 killing the toxic dinoflagellate Alexandrium tamarense. Sci Total Environ 482–483:116–124. https://doi.org/10.1016/j.scitotenv.2014.02.125
Zhang Q, Liu GX, Hu ZY (2011) Morphological observation of a freshwater Peridinium strain and phylogenetic analysis of Peridinium. Plant Sci J 29(1):1–10. https://doi.org/10.3724/sp.j.1142.2011.10001
Zhang BZ, Cai GJ, Wang HT, Li D, Yang XJ, An XL, Zheng XW, Tian Y, Zheng W, Zheng TL (2014a) Streptomyces alboflavus RPS and its novel and high algicidal activity against harmful algal bloom species Phaeocystis globosa. PLoS One 9(3):e92907. https://doi.org/10.1371/journal.pone.0092907
Zhang HJ, Lv JL, Peng Y, Zhang S, An XL, Xu H, Zhang J, Tian Y, Zheng W, Zheng TL (2014b) Cell death in a harmful algal bloom causing species Alexandrium tamarense upon an algicidal bacterium induction. Appl Microbiol Biotechnol 98(18):7949–7958. https://doi.org/10.1007/s00253-014-5886-1
Zhao L, Chen L, Yin P (2014) Algicidal metabolites produced by Bacillus sp. strain B1 against Phaeocystis globosa. J Ind Microbiol Biotechnol 41(3):593–599. https://doi.org/10.1007/s10295-013-1393-0
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We would like to thank Editage (www.editage.cn) for English language editing.
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This study was funded by the National Key R&D Program of China (2019YFD0900400); program of China Agriculture Research System (CARS-48); Central Public-Interest Scientific Institution Basal Research Fund, South China Sea Fisheries Research Institute, CAFS (2019TS06); Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams (2019KJ149); and Guangdong Special Fund for Economic Development Project (Modern Fisheries Development) (2019B12).
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Xiaojuan Hu performed the data analyses and wrote the manuscript, Haochang Su performed the analysis with discussions and helped to revise the manuscript,Yu Xu helped to perform the analysis with constructive discussions, Wujie Xu performed the experiments and analyzed the data, Shasha Li performed the experiments, Xiaoshuai Huang wrote the manuscript, Yucheng Cao and Guoliang Wen, as corresponding authors, designed the experiments and contributed to the conception of the study.
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Hu, X., Su, H., Xu, Y. et al. Algicidal properties of fermentation products from Bacillus cereus strain JZBC1 dissolving dominant dinoflagellate species Scrippsiella trochoidea, Prorocentrum micans, and Peridinium umbonatum. Biologia 75, 2015–2024 (2020). https://doi.org/10.2478/s11756-020-00500-3
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DOI: https://doi.org/10.2478/s11756-020-00500-3