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Adhesion and colonization properties of potentially probiotic Bacillus paralicheniformis strain FA6 isolated from grass carp intestine

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  • Aquaculture
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Abstract

As a prerequisite for probiotics to establish and settle in the host intestine, adhesion is an essential criterion for probiotic screening. However, adhesion of probiotics in the intestines of one of the most important cultured fish species globally, the grass carp Ctenopharyngodon idellus, remains understudied. Here, we assessed the adhesion properties of a novel potentially probiotic bacterial strain isolated from the grass carp intestine: Bacillus paralicheniformis FA6 (henceforth FA6). To indirectly determine the adhesion, we compared the hydrophobicity of FA6 with eight other bacterial strains, and found that FA6 had comparatively high hydrophobicity. To assess adhesion directly, we supplemented the feed with FA6 for 2 weeks, and then used immunofluorescence to study the dynamics of FA6 for 220 days after discontinuing the supplementation. The FA6 fluorescence signal plateaued between days 40 and 60, and remained visible in the grass carp guts until day 80. In addition, FA6 was re-isolated on day 220 from intestinal contents. Our results suggest that FA6 has high adhesion ability, and can colonize the grass carp intestine for long periods of time. This research provides a promising foundation for the application of FA6 in aquaculture.

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References

  • Aeby GS, Callahan S, Cox EF, Runyon C, Smith A, Stanton FG, Ushijima B, Work TM (2016) Emerging coral diseases in Kāne'ohe Bay, O'ahu, Hawai'i (USA): two major disease outbreaks of acute Montipora white syndrome. Dis Aquat Org 119:189–198

    Article  Google Scholar 

  • Alander M, Satokari R, Korpela R, Saxelin M, Vilpponen-Salmela T, Mattila-Sandholm T, Wright A (1999) Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol 65:351–355

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Argyri AA, Zoumpopoulou G, Karatzas KA, Tsakalidou E, Nychas GJ, Panagou EZ, Tassou CC (2013) Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol 33:282–291

    Article  CAS  Google Scholar 

  • Balcázar JL, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Muzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186

    Article  Google Scholar 

  • Bhadra R, Sandhya S, Abhinandan KR, Chakrabarti S, Sowdhamini R, Srinivasan N (2006) Cascade PSI-BLAST web server: a remote homology search tool for relating protein domains. Nucleic Acids Res 34:W143–W146

    Article  CAS  Google Scholar 

  • Buntin N, de Vos WM, Hongpattarakere T (2017) Variation of mucin adhesion, cell surface characteristics, and molecular mechanisms among Lactobacillus plantarum isolated from different habitats. Appl Microbiol Biotechnol 101:7663–7674

    Article  CAS  Google Scholar 

  • Dillon JK, Fuerst JA, Hayward AC, Davis GH (1986) A comparison of five methods for assaying bacterial hydrophobicity. J Microbiol Methods 6:13–19

    Article  CAS  Google Scholar 

  • Dunlap CA, Kwon SW, Rooney AP, Kim SJ (2015) Bacillus paralicheniformis sp. nov., isolated from fermented soybean paste. Int J Syst Evol Microbiol 65:3487–3492

    Article  CAS  Google Scholar 

  • Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H (2017) Bacillus as potential probiotics: status, concerns, and future perspectives. Front Microbiol 8:1490

    Article  Google Scholar 

  • FAO (2018) The state of world fisheries and aquaculture 2018-meeting the sustainable development goals. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Feng WW, Wu SG, Hao YT, Li WX, Li M, Zou H, Wang GT (2018) Isolation and identification of anaerobes in the intestinal mucosa of grass carp ctenopharyngodon idellus. Acta Hydrobiologica Sinica 42:11–16

    Google Scholar 

  • Ferreira GS, Bolívar NC, Pereira SA, Guertler C, Vieira FDN, Mouriño JLP, Seiffert WQ (2015) Microbial biofloc as source of probiotic bacteria for the culture of Litopenaeus vannamei. Aquaculture 448:273–279

    Article  CAS  Google Scholar 

  • Gatesoupe FJ (1999) The use of probiotics in aquaculture. Aquaculture 180:147–165

    Article  Google Scholar 

  • Hai NV, Fotedar R (2010) A review of probiotics in shrimp aquaculture. J Appl Aquacult 22:251–266

    Article  Google Scholar 

  • Han B, Long WQ, He JY, Liu YJ, Si YQ, Tian LX (2015) Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46:225–231

    Article  CAS  Google Scholar 

  • Hautefort I, Flechon B, Degrouard J, Fons M (2009) Adhesion to the digestive mucosa is not sufficient for durable persistence of different Lactobacillus fermentum strains in the digestive tract of mice. Microb Ecol Health Dis 12:48–56

    Article  Google Scholar 

  • Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) Expert consensus document: the International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Proc Natl Acad Sci USA 11:506–514

    Google Scholar 

  • Hoseinifar SH, Sun YZ, Wang A, Zhou Z (2018) Probiotics as means of diseases control in aquaculture, a review of current knowledge and future perspectives. Front Microbiol 9:2429

    Article  Google Scholar 

  • Husmark U, Rönner U (1992) The influence of hydrophobic, electrostatic and morphologic properties on the adhesion of Bacillus spores. Biofouling 5:335–344

    Article  CAS  Google Scholar 

  • Küpcü Z, März L, Messner P, Sleytr UB (1984) Evidence for the glycoprotein nature of the crystalline cell wall surface layer of Bacillus stearothermophilus strain NRS2004/3a. FEBS Lett 173:185–190

    Article  Google Scholar 

  • Kesarcodi-Watson A, Kaspar H, Lategan MJ, Gibson L (2008) Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture 274:1–14

    Article  Google Scholar 

  • Kohanski MA, Dwyer DJ, Collins JJ (2010) How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 8:423–435

    Article  CAS  Google Scholar 

  • Kos B, Susković J, Vuković S, Simpraga M, Frece J (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92. J Appl Microbiol 94:981–987

    Article  CAS  Google Scholar 

  • Kwok LY, Wang L, Zhang J, Guo Z, Zhang H (2014) A pilot study on the effect of Lactobacillus casei Zhang on intestinal microbiota parameters in Chinese subjects of different age. Benef Microbes 5:295–304

    Article  CAS  Google Scholar 

  • Mark Welch JL, Hasegawa Y, McNulty NP, Gordon JI, Borisy GG (2017) Spatial organization of a model 15-member human gut microbiota established in gnotobiotic mice. Proc Natl Acad Sci USA 114:E9105–E9114

    Article  CAS  Google Scholar 

  • Merrifield DL, Harper GM, Dimitroglou A, Einar R, Davies SJ (2010) Possible influence of probiotic adhesion to intestinal mucosa on the activity and morphology of rainbow trout (Oncorhynchus mykiss) enterocytes. Aquacult Res 41:1268–1272

    Google Scholar 

  • Ni DS, Wang JG (1999) Biology and diseases of grass carp. Science Press, Beijing

    Google Scholar 

  • Niu Y, Defoirdt T, Baruah K, Van de Wiele T, Dong S, Bossier P (2014) Bacillus sp. LT3 improves the survival of gnotobiotic brine shrimp (Artemia franciscana) larvae challenged with Vibrio campbellii by enhancing the innate immune response and by decreasing the activity of shrimp-associated vibrios. Vet Microbiol 173:279–288

    Article  CAS  Google Scholar 

  • Obuekwe CO, Al-Jadi ZK, Al-Saleh ES (2009) Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegrad 63:273–279

    Article  CAS  Google Scholar 

  • Rönner U, Husmark U, Henriksson A (1990) Adhesion of Bacillus spores in relation to hydrophobicity. J Appl Microbiol 69:550–556

    Google Scholar 

  • Romano A, Blaiotta G, Di Cerbo A, Coppola R, Masi P, Aponte M (2014) Spray-dried chestnut extract containing Lactobacillus rhamnosus cells as novel ingredient for a probiotic chestnut mousse. J Appl Microbiol 116:1632–1641

    Article  CAS  Google Scholar 

  • Sánchez B, Bressollier P, Urdaci MC (2008) Exported proteins in probiotic bacteria: adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. Pathog Dis 54:1–17

    Google Scholar 

  • Schillinger U, Guigas C, Holzapfel WH (2005) In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 15:1289–1297

    Article  CAS  Google Scholar 

  • Tran NT, Wang GT, Wu SG (2017) A review of intestinal microbes in grass carp Ctenopharyngodon idellus (Valenciennes). Aquacult Res 48:3287–3297

    Article  Google Scholar 

  • Van Loosdrecht M, Lyklema J, Norde W, Schraa G, Zehnder A (1987) The role of bacterial cell wall hydrophobicity in adhesion. Appl Environ Microbiol 53:1893–1897

    Article  Google Scholar 

  • Viegas MS, Martins TC, Seco F, Do Carmo A (2007) An improved and cost-effective methodology for the reduction of autofluorescence in direct immunofluorescence studies on formalin-fixed paraffin-embedded tissues. Eur J Basic Appl Histochem 51:59–66

    CAS  Google Scholar 

  • Wang B, Li J, Li Q, Zhang H, Li N (2009) Isolation of adhesive strains and evaluation of the colonization and immune response by Lactobacillus plantarum L2 in the rat gastrointestinal tract. Int J Food Microbiol 132:59–66

    Article  CAS  Google Scholar 

  • Wanka KM, Damerau T, Costas B, Krueger A, Schulz C, Wuertz S (2018) Isolation and characterization of native probiotics for fish farming. BMC Microbiol 18:119

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Pei Zhang and Du An-Na from the Core Facility and Technical Support, Wuhan Institute of Virology, for their help to produce TEM micrographs. This work was supported by National Key R&D Program of China (Grant No. 2018YFD0900400), National Natural Science Foundation of China (Grant No. 31872612) and the Earmarked Fund for China Agriculture Research System (Grant No. CARS-45-15). The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication.

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Authors and Affiliations

  1. Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, PR China

    Di Zhao, Shangong Wu, Wenwen Feng, Ngoc Tuan Tran & Fan Xiong

  2. University of Chinese Academy of Sciences, Beijing, 100049, PR China

    Di Zhao, Shangong Wu, Wenwen Feng & Fan Xiong

  3. Bio-Transduction Lab, Wuhan, 430075, China

    Ivan Jakovlić

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  1. Di Zhao
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  2. Shangong Wu
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  3. Wenwen Feng
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  4. Ivan Jakovlić
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  5. Ngoc Tuan Tran
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  6. Fan Xiong
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Correspondence to Shangong Wu.

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Zhao, D., Wu, S., Feng, W. et al. Adhesion and colonization properties of potentially probiotic Bacillus paralicheniformis strain FA6 isolated from grass carp intestine. Fish Sci 86, 153–161 (2020). https://doi.org/10.1007/s12562-019-01385-1

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  • DOI: https://doi.org/10.1007/s12562-019-01385-1

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