Skip to main content
SpringerLink
Log in

Effects of probiotic on microfloral structure of live feed used in larval breeding of turbot Scophthalmus maximus

  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The effects of an exogenous probiotic (Bacillus amyloliquefaciens) on microbial community structure of Branchionus plicatils and Artemia sinica were evaluated in this study during turbot (Scophthalmus maximus) larval breeding. The analysis and comparison of the microfloral composition of live feed with probiotic was conducted using the Illumina HiSeq PE250. The abundance of microbial species and diversity of microflora in live feed with B. amyloliquefaciens were higher than those in the control. The microfloral composition was similar among the three replicate experimental groups of B. plicatils compared with the control after enrichment. Lactococcus, Pseudoalteromonas, and Alteromonas were always dominant. Additionally, some other bacterial species became dominant during the enrichment process. The microbial community during nutrient enrichment of A. sinica was rather similar among the three control replicates. Relative abundance of Cobetia sp., the most dominant species, was 54%–65.2%. Similarity in the microbial community was still high after adding B. amyloliquefaciens. Furthermore, Pseudoalteromonas and Alteromonas replaced Cobetia as the dominant species, and the abundance of Cobetia decreased to 4.3%–25.3%. Mean common ratios at the operational taxonomic unit level were 50%–60% between the two B. plicatils and A. sinica treatments. Therefore, the microbial community structure changed after adding B. amyloliquefaciens during nutrient enrichment of B. plicatils or A. sinica and tended to stabilize. Additionally, the abundance of Vibrio in any kind of live feed was not significantly different from that in the control. These results will help improve the microflora of B. plicatils and A. sinica and can be used to understand the multiple-level transfer role of probiotic species among probiotic products, microflora of live feed, and fish larvae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmed Md S, Nour A M, Srour T M, Assem S, Ibrahim H A, El-Sayed H S. 2015. Greenwater, Marine Bacillus subtilis HS1 probiotic and synbiotic enriched artemia and rotifers improved European seabass Dicentrarchus labrax larvae early weaning length growth, survival, water and bacteriology quality. American Journal of Life Sciences, 3 (6–1): 45–52.

    Article  Google Scholar 

  • Allameh S K, Yusoff F M, Ringø E, Daud H M, Saad C R, Ideris A. 2016. Effects of dietary mono-and multiprobiotic strains on growth performance, gut bacteria and body composition of Javanese carp (Puntius gonionotus, Bleeker 1850). Aquaculture Nutrition, 22 (2): 367–373.

    Article  Google Scholar 

  • Asok A, Arshad E, Jasmin C, Pai S S, Singh I S B, Mohandas A, Anas A. 2012. Reducing Vibrio load in Artemia nauplii using antimicrobial photodynamic therapy: a promising strategy to reduce antibiotic application in shrimp larviculture. Microbial Biotechnology, 5 (1): 59–68.

    Article  Google Scholar 

  • Bakke I, Skjermo J, Vo T A, Vadstein O. 2013. Live feed is not a major determinant of the microbiota associated with cod larvae (Gadus morhua). Environmental M icrobiology Reports, 5 (4): 537–548.

    Article  Google Scholar 

  • Battaglene S C, Morehead D T, Cobcroft J M, Nichols P D, Brown M R, Carson J. 2006. Combined effects of feeding enriched rotifers and antibiotic addition on performance of striped trumpeter (Latris lineata) larvae. Aquaculture, 251 (2–4): 456–471.

    Article  Google Scholar 

  • Bergh Ø, Naas K E, Harboe T. 1994. Shift in the intestinal microflora of Atlantic halibut (Hippoglossus hippoglossus) larvae during first feeding. Canadian Journal of Fisheries and Aquatic Sciences, 51 (8): 1 899–1 903.

    Article  Google Scholar 

  • Cai Y M, Benno Y, Nakase T, Oh T K. 1998. Specific probiotic characterization of Weissella hellenica DS-12 isolated from flounder intestine. The Journal of General and Applied Microbiology, 44 (5): 311–316.

    Article  Google Scholar 

  • Campbell R, Adams A, Tatner M F, Chair M, Sorgeloos P. 1993. Uptake of Vibrio anguillarum vaccine by Artemia salina as a potential oral delivery system to fish fry. Fish & Shellfish Immun ology, 3 (6): 451–459.

    Article  Google Scholar 

  • Cao H P, He S, Wei R P, Diong M, Lu L Q. 2011. Bacillus amyloliquefaciens G1: a potential antagonistic bacterium against eel-pathogenic A eromonas hydrophila. Evidence-Based Complementary and Alternative Medicine, 2011: 824104.

    Google Scholar 

  • Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. Qiime allows analysis of high-throughput community sequencing data. Nature Methods, 7 (5): 335–336.

    Article  Google Scholar 

  • Carnevali O, Zamponi M C, Sulpizio R, Rollo A, Nardi M, Orpianesi C, Silvi S, Caggiano M, Polzonetti A M, Cresci A. 2004. Administration of probiotic strain to improve sea bream wellness during development. Aquaculture International, 12 (4–5): 377–386.

    Article  Google Scholar 

  • Chambers J R, Gong J. 2011. The intestinal microbiota and its modulation for Salmonella control in chickens. Food Research International, 44 (10): 3 149–3 159.

    Article  Google Scholar 

  • Chen S C, Liaw L L, Su H Y, Ko S C, Wu C Y, Chaung H C, Tsai Y H, Yang K L, Chen Y C, Chen T H, Lin G R, Cheng S Y, Lin Y D, Lee J L, Lai C C, Weng Y J, Chu S Y. 2002. Lactococcus garvieae, a cause of disease in grey mullet, Mugil cephalus L., in Taiwan. Journal of Fish Diseases, 25 (12): 727–732.

    Article  Google Scholar 

  • Chen S C, Lin Y D, Liaw L L, Wang P C. 2001. Lactococcus garvieae infection in the giant freshwater prawn Macrobranchium rosenbergii confirmed by polymerase chain reaction and 16S rDNA sequencing. Diseases of Aquatic Organisms, 45 (1): 45–52.

    Article  Google Scholar 

  • Das A, Nakhro K, Chowdhury S, Kamilya D. 2013. Effects of potential probiotic B acillus amyloliquifaciens fptb16 on systemic and cutaneous mucosal immune responses and disease resistance of catla (Catla catla). Fish & Shellfish Immunology, 35 (5): 1 547–1 553.

    Article  Google Scholar 

  • Defoirdt T, Halet D, Vervaeren H, Boon N, Van de Wiele T, Sorgeloos P, Bossier P, Verstraete W. 2007. The bacterial storage compound poly-β-hydroxybutyrate protects Artemia franciscana from pathogenic Vibrio campbellii. Environmental Microbiology, 9 (2): 445–452.

    Article  Google Scholar 

  • Díaz-Rosales P, Salinas I, Rodríguez A, Cuesta A, Chabrillón M, Balebona M C, Moriñigo M Á, Esteban M Á, Meseguer J. 2006. Gilthead seabream (Sparus aurata L.) innate immune response after dietary administration of heatinactivated potential probiotics. Fish & Shellfish Immunology, 20 (4): 482–492.

    Article  Google Scholar 

  • Diaz-Sanchez S, Hanning I, Pendleton S, D’Souza D. 2013. Next-generation sequencing: the future of molecular genetics in poultry production and food safety. Poultry Science, 92 (2): 562–572.

    Article  Google Scholar 

  • Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27 (16): 2 194–2 200.

    Article  Google Scholar 

  • Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10 (10): 996–998.

    Article  Google Scholar 

  • Fan R F. 2010. Screening of potential probiotics derived from intestine of cultured Scophthalmus maximus and preliminary application. Shanghai Ocean University, Shanghai. (in Chinese with English abstract)

    Google Scholar 

  • Fang H, Wang H F, Cai L, Yu Y L. 2015. Prevalence of antibiotic resistance genes and bacterial pathogens in long-term manured greenhouse soils as revealed by metagenomic survey. Environmental Science & Technology, 49 (2): 1 095–1 104.

    Article  Google Scholar 

  • Ferguson H W, Collins R O, Moore M, Coles M, MacPhee D D. 2004. Pseudomonas anguilliseptica infection in farmed cod, Gadus morhua L. Journal of F ish Diseases, 27 (4): 249–253.

    Article  Google Scholar 

  • Garcés M E, Sequeiros C, Olivera N L. 2015. Marine Lactobacillus pentosus H16 protects Artemia franciscana from Vibrio alginolyticus pathogenic effects. Diseases of Aquatic Organisms, 113 (1): 41–50.

    Article  Google Scholar 

  • Garnier M, Labreuche Y, Garcia C, Robert M, Nicolas J L. 2007. Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microbial Ecology, 53 (2): 187–196.

    Article  Google Scholar 

  • Gatesoupe F J. 1990. The continuous feeding of turbot larvae, Scophthalmus maximus, and control of the bacterial environment of rotifers. Aquaculture, 89 (2): 139–148.

    Article  Google Scholar 

  • Gatesoupe F J. 1991. Managing the dietary value of Artemia for larval turbot, Scophthalmus maximus; the effect of enrichment and distribution techniques. Aquacultural Engineering, 10 (2): 111–119.

    Article  Google Scholar 

  • Gatesoupe F J. 1994. Lactic acid bacteria increase the resistance of turbot larvae, Scophthalmus maximus, against pathogenic Vibrio. Aquatic Living Resources, 7 (4): 277–282.

    Article  Google Scholar 

  • Gatesoupe F J. 2002. Probiotic and formaldehyde treatments of Artemia nauplii as food for larval pollack, Pollachius pollachius. Aquaculture, 212 (1–4): 347–360.

    Article  Google Scholar 

  • Gatesoupe F J. 2008. Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments. Journal of M olecular M icrobiology and B iotechnology, 14 (1–3): 107–114.

    Google Scholar 

  • Gianelli J D, Kennedy S B, Fernandez E M, Gensler A L, Tucker J W J. 1997. Increased production of rotifers treated with Bacillus sp. isolated from common snook (Ce n tropom o us undec emalis) larvae. World Aquaculture, 97: 131.

    Google Scholar 

  • Hjelm M, Bergh Ø, Riaza A, Nielsen J, Melchiorsen J, Jensen S, Duncan H, Ahrens P, Birkbeck H, Gram L. 2004. Selection and identification of autochthonous potential probiotic bacteria from turbot larvae (Scophthalmus maximus) rearing units. Systematic and Applied Microbiology, 27 (3): 360–371.

    Article  Google Scholar 

  • Hoshina T, Sano T, Morimoto Y. 1958. A Streptococcus pathogenic to fish. Journal of the Tokyo Univ ersity of Fish eries, 44: 44–57.

    Google Scholar 

  • Huys G, Bartie K, Cnockaert M, Oanh D T H, Phuong N T, Somsiri T, Chinabut S, Yusoff F M, Shariff M, Giacomini M, Teale A, Swings J. 2007. Biodiversity of chloramphenicol-resistant mesophilic heterotrophs from Southeast Asian aquaculture environments. Research in M icrobiology, 158 (3): 228–235.

    Google Scholar 

  • Huys L, Dhert P, Robles R, Ollevier F, Sorgeloos P, Swings J. 2001. Search for beneficial bacterial strains for turbot (Scophthalmus maximus L.) larviculture. Aquaculture, 193 (1–2): 25–37.

    Article  Google Scholar 

  • Immanuel G, Citarasu T, Sivaram V, Babu M M, Palavesam A. 2007. Delivery of HUFA, probionts and biomedicine through bioencapsulated Artemia as a means to enhance the growth and survival and reduce the pathogenesity in shrimp Penaeus monodon postlarvae. Aquaculture International, 15 (2): 137–152.

    Article  Google Scholar 

  • Jamali H, Imani A, Abdollahi D, Roozbehfar R, Isari A. 2015. Use of probiotic Bacillus spp. in rotifer (Brachionus plicatilis) and artemia (Artemia urmiana) enrichment: effects on growth and survival of pacific white shrimp, Litopenaeus vannamei, larvae. Probiotics and Antimicrobial Proteins, 7 (2): 118–125.

    Article  Google Scholar 

  • Kim D H, Austin B. 2006. Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish & Shellfish Immunology, 21 (5): 513–524.

    Article  Google Scholar 

  • Lamari F, Sadok K, Bakhrouf A, Gatesoupe F J. 2014. Selection of lactic acid bacteria as candidate probiotics and in vivo test on Artemia nauplii. Aquaculture International, 22 (2): 699–709.

    Article  Google Scholar 

  • Magi G E, Lopez-Romalde S, Magariños G E, Lamas J, Toranzo A E, Romalde J L. 2009. Experimental Pseudomonas anguilliseptica infection in turbot Psetta maxima (L.): a histopathological and immunohistochemical study. European Journal of Histochemistry, 53 (2): e9.

    Article  Google Scholar 

  • Martínez-Díaz S F, Álvarez-González C A, Legorreta M M, Vázquez-Juárez R, Barrios-González J. 2003. Elimination of the associated microbial community and bioencapsulation of bacteria in the rotifer Brachionus plicatilis. Aquaculture International, 11 (1–2): 95–108.

    Article  Google Scholar 

  • Munro P D, Barbour A, Birkbeck T H. 1995. Comparison of the growth and survival of larval turbot in the absence of culturable bacteria with those in the presence of Vibrio anguillarum, Vibrio alginolyticus, or a marine Aeromonas sp. Applied and Environmental Microbiology, 61 (12): 4 425–4 428.

    Google Scholar 

  • Nayak S K. 2010. Probiotics and immunity: a fish perspective. Fish & Shellfish Immunology, 29 (1): 2–14.

    Article  Google Scholar 

  • Palma J, Bureau D P, Andrade J P. 2011. Effect of different Artemia enrichments and feeding protocol for rearing juvenile long snout seahorse, Hippocampus guttulatus. Aquaculture, 318 (3–4): 439–443.

    Article  Google Scholar 

  • Planas M, Pérez-Lorenzo M, Hjelm M, Gram L, Fiksdal I U, Bergh Ø, Pintado J. 2006. Probiotic effect in vivo of Roseobacter strain 27–4 against Vibrio (Listonella) anguillarum infections in turbot (Scophthalmus maximus L.) larvae. Aquaculture, 255 (1–4): 323–333.

    Article  Google Scholar 

  • Ruscoe I M, Williams G R, Shelley C C. 2004. Limiting the use of rotifers to the first zoeal stage in mud crab (Scylla serrata Forskål) larval rearing. Aquaculture, 231 (1–4): 517–527.

    Article  Google Scholar 

  • Shi X Q, Zhang Z, Wang Y G, Yu Y X, Deng W, Li H. 2015. The characteristics of culturable bacterial microflora in the gastrointestinal tract of turbot (Scophthatmus maximus) larvae. Progress i n Fishery Sciences, 36 (4): 73–82. (in Chinese with English abstract)

    Google Scholar 

  • Shiri Harzevili A R, van Duffel H, Dhert P, Swings J, Sorgeloos P. 1998. Use of a potential probiotic Lactococcus lactis AR21 strain for the enhancement of growth in the rotifer Brachionus plicatilis (Müller). Aquaculture Research, 29 (6): 411–417.

    Google Scholar 

  • Silva E F, Soares M A, Calazans N F, Vogeley J L, do Valle B C, Soares R, Peixoto S. 2012. Effect of probiotic (Bacillus spp.) addition during larvae and postlarvae culture of the white shrimp Litopenaeus vannamei. Aquaculture Research, 44 (1): 13–21.

    Article  Google Scholar 

  • Skjermo J, Bakke I, Dahle S W, Vadstein O. 2015. Probiotic strains introduced through live feed and rearing water have low colonizing success in developing Atlantic cod larvae. Aquaculture, 438: 17–23.

    Article  Google Scholar 

  • Smith P, Hiney M P, Samuelsen O B. 1994. Bacterial resistance to antimicrobial agents used in fish farming: a critical evaluation of method and meaning. Annual Review of Fish Diseases, 4: 4–273.

    Article  Google Scholar 

  • Subasinghe R. 1997. Fish health and quarantine. In: Review of the State of the World Aquaculture—FAO Fisheries Circular no.886. Food and Agriculture Organization of the United Nations, Rome. p.45-49.

    Google Scholar 

  • Suga K, Tanaka Y, Sakakura Y, Hagiwara A. 2011. Axenic culture of Brachionus plicatilis using antibiotics. Hydrobiologia, 662 (1): 113–119.

    Article  Google Scholar 

  • Sulkin S D, Epifanio C E. 1975. Comparison of rotifers and other diets for rearing early larvae of the blue crab, Callinectes sapidus Rathbun. Estuarine and Coastal Marine Science, 3 (1): 109–113.

    Article  Google Scholar 

  • Sun Y Z, Yang H L, Huang K P, Ye J D, Zhang C X. 2013. Application of autochthonous Bacillus bioencapsulated in copepod to grouper Epinephelus coioides larvae. Aquaculture, 392-395: 44–50.

    Article  Google Scholar 

  • Verschuere L, Heang H, Criel G, Dafnis S, Sorgeloos P, Verstraete W. 2000a. Selected bacterial strains protect Artemia spp. from the Pathogenic Effects of Vibrio proteolyticus CW8T2. Appl ied and Environ mental Microbiol ogy, 66 (3): 1 139–1 146.

    Article  Google Scholar 

  • Verschuere L, Rombaut G, Sorgeloos P, Verstraete W. 2000b. Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews, 64 (4): 655–671.

    Article  Google Scholar 

  • Villamil L, Figueras A, Planas M, Novoa B. 2003. Control of Vibrio alginolyticus in Artemia culture by treatment with bacterial probiotics. Aquaculture, 219 (1–4): 43–56.

    Article  Google Scholar 

  • Wang S X, Yang Z X, Sun Z, Liu Y, Wang C W, Jing Y H. 2014. Application of high throughput sequencing in the diversity of water microbial communities. Chemistry, 77 (3): 196–203. (in Chinese with English abstract)

    Google Scholar 

  • Wu Z Q, Jiang C, Ling F, Wang G X. 2015. Effects of dietary supplementation of intestinal autochthonous bacteria on the innate immunity and disease resistance of grass carp (Ctenopharyngodon idellus). Aquaculture, 438: 105–114.

    Article  Google Scholar 

  • Zhang Z, Liao M J, Li B, Wang Y G, Wang L, Rong X J, Chen G P. 2014. Study on cultured half-smooth tongue sole (Cynoglossus semilaevis Günther) intestinal microflora changes affected by different disease occurrence. Journal of Fisheries of China, 38 (9): 1 565–1 572. (in Chinese with English abstract)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Yan Jiang  (姜燕), Zheng Zhang  (张正), Yingeng Wang  (王印庚), Yayun Jing  (景亚运), Meijie Liao  (廖梅杰), Xiaojun Rong  (荣小军), Bin Li  (李彬) & Guiping Chen  (陈贵平)

  2. Qingdao General Aquatic Co. Ltd., Qingdao, 266000, China

    Hesen Zhang  (张和森)

Authors
  1. Yan Jiang  (姜燕)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zheng Zhang  (张正)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yingeng Wang  (王印庚)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yayun Jing  (景亚运)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Meijie Liao  (廖梅杰)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaojun Rong  (荣小军)
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bin Li  (李彬)
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guiping Chen  (陈贵平)
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hesen Zhang  (张和森)
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yingeng Wang  (王印庚).

Additional information

Supported by the National Natural Science Foundation of China (No. 31302206) and the Postdoctoral Applied Research Project of Qingdao (No. Q51201607)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiang, Y., Zhang, Z., Wang, Y. et al. Effects of probiotic on microfloral structure of live feed used in larval breeding of turbot Scophthalmus maximus. J. Ocean. Limnol. 36, 1002–1012 (2018). https://doi.org/10.1007/s00343-018-7049-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-018-7049-1

Keyword

Search

Navigation