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Effects of Bacillus subtilis on the growth, colony maintenance, and attached bacterial community composition of colonial cyanobacteria

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Abstract

In freshwater aquaculture ponds, application of algicidal Bacillus is a promising way in the control of cyanobacterial blooms. To best understand Bacillus algicidal characters and mechanisms in the field, different-sized colonial cyanobacteria were isolated from an aquaculture pond, and the effects of B. subtilis on their growth, colony maintenance, and colony-attached bacterial community composition were investigated. The results showed that B. subtilis could inhibit the growth of colonial cyanobacteria. Bigger-sized colonies isolated from the field could spontaneously disintegrate into smaller-sized colonies in the laboratory. Algicidal B. subtilis could accelerate the disintegration of colonies and decrease colony size. B. subtilis not only decreased the colony-attached bacterial community diversity but also changed its composition. B. subtilis increased the relative abundances of some attached bacterial genera, including Pseudomonas, Shewanella, Bacillus, Shinella, Rhizobium, and Ensifer. These bacteria with algicidal, microcystin-degrading, and flocculating activities might be an important contributor to algicidal effects of B. subtilis on colonial cyanobacteria.

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References

  • Balcázar JL, Rojas-Luna T, Cunningham DP (2007) Effect of the addition of four potential probiotic strains on the survival of pacific white shrimp (Litopenaeus vannamei) following immersion challenge with Vibrio parahaemolyticus. J Invertebr Pathol 96:147–150

    Article  Google Scholar 

  • Bi XD, Zhang SL, Dai W et al (2013) Effects of lead (II) on the extracellular polysaccharide (EPS) production and colony formation of cultured Microcystis aeruginosa. Water Sci Technol 67:803–809

    Article  CAS  Google Scholar 

  • Bi XD, Dai W, Zhang SL et al (2017) Effects of toxic Microcystis genotypes in natural colony formation and mechanism involved. Water Sci Technol 76:885–894

    Article  CAS  Google Scholar 

  • Bokulich NA, Nicholas A, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illuminaamplicon sequencing. Nat Methods 10:57–59

    Article  CAS  Google Scholar 

  • Bolch CJS, Blackburn SI (1996) Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz. J Appl Phycol 8:5–13

    Article  Google Scholar 

  • Boström B, Pettersson AK, Ahlgren I (1989) Seasonal dynamics of a cyanobacteria-dominated microbial community in surface sediments of a shallow eutrophic lake. Aquat Sci 51:153–178

    Article  Google Scholar 

  • Brunberg AK (1999) Contribution of bacteria in the mucilage of Microcystis spp. (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol Ecol 29:13–22

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522

    Article  Google Scholar 

  • Chen YW, Qing BQ, Teubner K (2003) Long-term dynamics of phytoplankton assemblages: Microcystisdomination in Lake Taihu, a large shallow lake in China. J Plankton Res 25: 445–453

  • Cutting SM (2011) Bacillus probiotics. Food Microbiol 28:214–220

    Article  Google Scholar 

  • Desantis TZ, Hugenholtz P, Larsen N et al (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  Google Scholar 

  • Edgar RC, Robert C, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  Google Scholar 

  • Frangeul L, Quillardet P, Castets AM et al (2008) Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9:274

    Article  CAS  Google Scholar 

  • Fuks D, Radic J, Radic T et al (2005) Relationships between heterotrophic bacteria and cyanobacteria in the northern Adriatic in relation to the mucilage phenomenon. Sci Total Environ 353:178–188

    Article  CAS  Google Scholar 

  • Gan NQ, Xiao Y, Zhu L et al (2012) The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ Microbiol 14:730–742

    Article  CAS  Google Scholar 

  • Haas BJ, Gevers D, Earl AM et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  CAS  Google Scholar 

  • Hu HJ, Wei YX (2006) The Freshwater Algae of China: Systematics, Taxonomy and Ecology. Science Press, Beijing

    Google Scholar 

  • Hu X, Zhang R, Ye J et al (2017) Monitoring and research of microcystins and environmental factors in a typical artificial freshwater aquaculture pond. Environ Sci Pollut Res 4:1–13

    Google Scholar 

  • Jiang LJ, Yang LY, Xiao L et al (2007) Quantitative studies on phosphorus transference occurring between Microcystis aeruginosa and its attached bacterium (Pseudomonas sp.). Hydrobiologia 581:161–165

    Article  CAS  Google Scholar 

  • Kim SJ, Lee SS (2009) Growth suppression of Microcystis aeruginosa by Pseudomonas aeruginosa AJ1. Korean J Microbiol 45:362–367

    Google Scholar 

  • Kim HS, Ahn CY, Joung SH et al (2010) Growth inhibition of Microcystis aeruginosa by a glycolipid-type compound from Bacillus subtilis C1. J Microbiol Biotechnol 20:1240–1242

    Article  CAS  Google Scholar 

  • Kurmayer R, Christiansen G, Chorus I (2003) The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Appl Environ Microbiol 69:787–795

    Article  CAS  Google Scholar 

  • Li Z, Lin S, Liu X et al (2014) A freshwater bacterial strain, Shewanella sp. Lzh-2, isolated from Lake Taihu and its two algicidal active substances, hexahydropyrrolo[1,2-a]pyrazine-1,4-dione and 2, 3-indolinedione. Appl Microbiol Biot 98:4737–4748

    Article  CAS  Google Scholar 

  • Li Z, Geng M, Yang H (2015) Algicidal activity of Bacillus sp. Lzh-5 and its algicidal compounds against Microcystis aeruginosa. Appl Microbiol Biotechnol 99:1–10

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  CAS  Google Scholar 

  • Manage PM, Kawabata Z, Nakano S (2001) Dynamics of cyanophage-like particles and algicidal bacteria causing Microcystis aeruginosa mortality. Limnology 2:73–78

    Article  Google Scholar 

  • Maruyama T, Kato K, Yokoyama A et al (2003) Dynamics of microcystindegrading bacteria in mucilage of Microcystis. Microb Ecol 46:279–288

    Article  CAS  Google Scholar 

  • Mu RM, Fan ZQ, Pei HY et al (2007) Isolation and algae-lysing characteristics of the algicidal bacterium B5. J Environ Sci (China) 19:1336–1340

    Article  CAS  Google Scholar 

  • Ozaki K, Ohta A, Iwata C et al (2008) Lysis of cyanobacteria with volatile organic compounds. Chemosphere 71:1531–1538

    Article  CAS  Google Scholar 

  • Paerl HW, Tucker CS (2010) Ecology of Bluegreen Algae in Aquaculture Ponds. J World Aquacult Soc 26:109–131

  • Qi ZZ, Zhang XH, Boon N et al (2009) Probiotics in aquaculture of China — current state, problems and prospect. Aquaculture 290:15–21

    Article  Google Scholar 

  • Ramani A, Rein K, Shetty KG et al (2012) Microbial degradation of microcystin in Florida’s freshwaters. Biodegradation 23:35–45

    Article  CAS  Google Scholar 

  • Rinta-Kanto JM, Ouellette AJ, Boyer GL et al (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Environ Sci Technol 39:4198–4205

  • Sha T, Wei DJ, Chang YT et al (2017) Aerobic biodegradation of microcystin-LR by an indigenous bacterial mixed culture isolated in Taiwan. Int Biodeter Biodeger 124:101–108

  • Shao J, Jiang Y, Wang Z (2014) Interactions between algicidal bacteria and the cyanobacterium Microcystis aeruginosa: lytic characteristics and physiological responses in the cyanobacteria. Int J Environ Sci Technol 11:469–476

    Article  CAS  Google Scholar 

  • Shao JH, He YX, Chen AW et al (2015) Interactive effects of algicidal efficiency of Bacillus sp. B50 and bacterial community on susceptibility of Microcystis aeruginosa with different growth rates. Int Biodeter Bodidegr 97:1–6

    Article  Google Scholar 

  • Shen H, Niu Y, Xie P et al (2011) Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biol 56:1065–1080

    Article  CAS  Google Scholar 

  • Shi SY, Liu YD, Shen YW et al (2006) Lysis of Aphanizomenon Xos-aquae (Cyanobacterium) by a bacterium Bacillus cereus. Biol Control 39:345–351

    Article  CAS  Google Scholar 

  • Song ZF, An J, Fu GH (2011) Isolation and characterization of an aerobic denitrifying Bacillus sp. YX-6 from shrimp culture ponds. Aquaculture 319:188–193

    Article  CAS  Google Scholar 

  • Steppe TF, Olson JB, Paerl HW et al (1996) Consortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21:149–156

    Article  CAS  Google Scholar 

  • Vaitomaa J, Rantala A, Halinen K et al (2003) Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Appl Environ Microbiol 69:7289–7297

    Article  CAS  Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P et al (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Wang XY, Xie MJ, Wu W et al (2013) Differential sensitivity of colonial and unicellular Microcystis strains to an algicidal bacterium Pseudomonas aeruginosa. J Plankton Res 35:1172–1176

    Article  Google Scholar 

  • Wang WJ, Zhang YL, Shen H et al (2015) Changes in the bacterial community and extracellular compounds associated with the disaggregation of Microcystis colonies. Biochem Syst Ecol 61:62–66

    Article  CAS  Google Scholar 

  • Wang W, Shen H, Shi P et al (2016) Experimental evidence for the role of heterotrophic bacteria in the formation of Microcystis colonies. J Appl Phycol 28:1111–1123

    Article  CAS  Google Scholar 

  • Whitton BA (1973) Interactions with other organisms. In: Carr NG, Whitton BA (eds) The Biology of Blue-green Algae. Blackwell, Oxford, pp 415–433

    Google Scholar 

  • Worm J, Søndergaard M (1998) Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquat Microb Ecol 14(1):19–28

    Article  Google Scholar 

  • Wu ZX, Gan NQ, Huang Q et al (2007) Response of Microcystis to copper stress - do phenotypes of Microcystis make a difference in stress tolerance? Environ Pollut 147:324–330

    Article  CAS  Google Scholar 

  • Xiao Y, Gan NQ, Liu J et al (2012) Heterogeneity of buoyancy in response to light between two buoyant types of cyanobacterium Microcystis. Hydrobiologia 679:297–311

    Article  Google Scholar 

  • Xu YT, Yi L, Zhao GW et al (2017) Flocculation effect of Shinella sp. xn-1 on Microcystis aeruginosa. Microbiol China 44:1808–1816 (In Chinese)

    Google Scholar 

  • Yang Z, Kong FX (2012) Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. J Limnol l71:61–66

    Google Scholar 

  • Yang Z, Kong FX, Shi XL et al (2008) Changes in the morphology and polysaccharide content of Microcystis aeruginosa (Cyanobacteria) during flagellate grazing. J Phycol 44:716–720

    Article  Google Scholar 

  • Yoshida M, Yoshida T, Takashima Y et al (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266:49–53

    Article  CAS  Google Scholar 

  • Yu GL, Song LR, Li RH (2007) Taxonomic notes on water bloom forming Microcystis species (Cyanophyta) from China—an example from samples of the Dianchi Lake. Acta Phytotaxon Sin 45:727–741

    Article  Google Scholar 

  • Zhang B, Zhang SL, Chen CX (2009) Review on chemical control of Microcystis. J Hydroecol 2:124–128

    Google Scholar 

  • Zhao Y, Zhang W, Xu W et al (2012) Effects of potential probiotic Bacillus subtilis T13 on growth, immunity and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish Shellfish Immun 32:750–755

    Article  CAS  Google Scholar 

  • Zhou S, Yin H, Tang S et al (2016) Physiological responses of Microcystis aeruginosa against the algicidal bacterium Pseudomonas aeruginosa. Ecotoxicol Environ Saf 127:214–221

  • Zhu X, Shen Y, Chen X et al (2016) Biodegradation mechanism of microcystin-LR by a novel isolate of Rhizobium sp. TH and the evolutionary origin of the mlrA gene. Int Biodeter Bodidegr 115:17–25

    Article  CAS  Google Scholar 

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Funding

This study was financially supported by the National Natural Science Foundation of China (Grant No. 31772857 and 31640009), the Natural Science Foundation Grant of Tianjin (Grant Nos. 17JCYBJC29500 and 16JCYBJC29900), the Modern Aqua-ecology and Health Aquaculture Innovation Team of Tianjin (Grant No. TD-135089), and the Tianjin Agricultural University Key Laboratory of Aqua-ecology platform project (Grant No. 02).

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  1. Key Laboratory of Aquatic-Ecology and Aquaculture of Tianjin, Department of Fisheries Sciences, Tianjin Agricultural University, Jinjing Road No.22, Xiqing District, Tianjin, 300384, China

    Xiangdong Bi, Wei Dai, Xueying Wang, Shaojie Dong, Shulin Zhang, Dajuan Zhang & Hongyue Shi

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  1. Xiangdong Bi
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  2. Wei Dai
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  7. Hongyue Shi
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Correspondence to Xiangdong Bi.

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Bi, X., Dai, W., Wang, X. et al. Effects of Bacillus subtilis on the growth, colony maintenance, and attached bacterial community composition of colonial cyanobacteria. Environ Sci Pollut Res 26, 14977–14987 (2019). https://doi.org/10.1007/s11356-019-04902-y

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