Skip to main content
SpringerLink
Log in

Identification of a Proteus penneri isolate as the causal agent of red body disease of the cultured white shrimp Penaeus vannamei and its control with Bdellovibrio bacteriovorus

  • Short Communication
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Bacteriosis has become a major economic problem in the farming of the Pacific white shrimp Penaeus vannamei. However, no definitive data are available about Proteus penneri infection in cultured P. vannamei and its control. In this study, a virulent strain NC was isolated from diseased P. vannamei suffering from red body disease and identified as a P. penneri isolate through phylogenetic analysis and ATB 32GN system. A phylogenetic constructed tree using the neighbour-joining method identified the NC isolate as a P. penneri strain. In addition, Bdellovibrio bacteriovorus conferred significant protection against P. penneri: it exhibited significant bacteriolytic effects on the pathogenic P. penneri, had a wide prey range towards Proteus pathogens, and displayed a good protective efficacy on experimental P. penneri infection in P. vannamei. To the best of our knowledge, this is the first report of farmed P. vannamei infected with P. penneri and its control with B. bacteriovorus.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Alapide-Tendencia EV, Dureza LA (1997) Isolation of Vibrio spp. from Penaeus monodon (Fabricius) with red disease syndrome. Aquaculture 154(2):107–114

    Article  Google Scholar 

  • Altwegg M, Zollinger-Iten J (1987) Identification of Enterobacteriaceae, Aeromonas spp. and Plesiomonas shigelloides with ATB 32GN system. J Microbiol Meth 7:103–109

    Article  Google Scholar 

  • Baulny MOD, Quentel C, Fournier V, Lamour F, Gouvello RL (1996) Effect of long-term oral administration of β-glucan as an immunostimulant or an adjuvant on some non-specific parameters of the immune response of turbot Scophthalmus maximus. Dis Aquat Organ 26:139–147

    Article  Google Scholar 

  • Briggs M, Funge-Smith S, Subasinghe R, Phillips M (2004) Introductions and movement of Penaeus vannamei and Penaeus stlirostris in Asia and the Pacific. FAO Fisheries Technical Paper, 1-12 pp

  • Bucke D (1989) Histology. In: Austin B, Austin DA (eds) Methods for the microbiological examination of fish and shellfish. Wiley, New York, pp 69–97

    Google Scholar 

  • Cao H, Li Y, Lei Y, Wu J, Xu H (2007) Isolation, identification, phylogenetic analysis and related properties of a pathogen in Silurus meridionalis Chen. Acta Microbiol Sin 47(1):1–6

    CAS  Google Scholar 

  • Cao H, He S, Lu L, Hou L (2010) Characterization and phylogenetic analysis of the bitrichous pathogenic Aeromonas hydrophila isolated from diseased Siberian sturgen (Acipenser baerii). Isr J Aquacult-Bamid 62:182–189

    Google Scholar 

  • Cao H, He S, Wang H, Hou S, Lu L, Yang X (2012) Bdellovibrios, potential biocontrol bacteria against pathogenic Aeromonas hydrophila. Vet Microbiol 154:413–418

    Article  PubMed  Google Scholar 

  • Chen J, Zhu N, Kong L, Ding X, Zheng T, Du J (2012) Molecular characteristics and antimicrobial sensitivity of bacterial pathogen from the outbreak of Litopenaeus vannamei red-body disease. J Fish China 36(12):1891–1900

    CAS  Google Scholar 

  • Crossman LC, Chen H, Cerdeńo-Tárraga A, Brooks K, Quail MA, Pineiro SA, Hobley L, Sockett RE, Bentley SD, Parkhill J, Williams HN, Stine OC (2013) A small predatory core genome in the divergent marine Bacteriovorax marinus SJ and the terrestrial Bdellovibrio bacteriovorus. ISME J 7:148–160

    Article  CAS  PubMed  Google Scholar 

  • Dong XZ, Cai MY (2001) General manual of systematic and determinative bacteriology. Science Press, Beijing 97 pp

    Google Scholar 

  • Engler HD, Troy K, Bottone EJ (1990) Bacteremia and subcutaneous abscess caused by Proteus penneri in a neutropenic host. J Clin Microbiol 28:1645–1646

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fan JF, Li WZ, Zang HM, Wang B, Song L (2006) The pathogen of red body disease in Litopenaeus vannamei. Acta Hydrobiol Sin 30(6):742–746

    CAS  Google Scholar 

  • Felix F, Nugroho T, Silalahi S, Octavia Y (2011) Molecular characteristics of Vibrio sp. causing Black Tiger Prawn (Penaeus monodon) disease in Sumatra and Java shrimp ponds by 16S rDNA sequencing. J Agr Tech 7(3):679–694

    Google Scholar 

  • Geng Y, Wang K, Chen D, Huang X, He M, Yin Z (2010) Stemptrophomonas maltophilia, an emerging opportunist pathogen for cultured channel catfish, Ictalurus punctatus, in China. Aquaculture 308:132–135

    Article  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo M (2010) Effect of probiotics enriched diet on Paralichthys olivaceus infected with lymphocystis disease virus (LCDV). Fish Shellfish Immunol 29:868–874

    Article  PubMed  Google Scholar 

  • Jayasinghe CVL, Ahmed SBN, Kariyawasam MGIU (2008) The isolation and identification of Vibrio species in marine shrimps of Sri Lanka. J Food Agric 1(1):36–44

    Google Scholar 

  • Jayasree L, Janakiram P, Madhavi R (2006) Characterization of Vibrio spp. associated with diseased shrimp from culture ponds of Andhra Pradesh (India). J World Aquacult Soc 37(4):523–532

    Article  Google Scholar 

  • Kaistha N, Bansal N, Chander J (2011) Proteus penneri lurking in the intensive care unit: an important often ignored nosocomial pathogen. Indian J Anaesth 55:411–413

    Article  PubMed Central  PubMed  Google Scholar 

  • Kishore J (2012) Isolation, identification & characterization of Proteus penneri-a missed rare pathogen. Indian J Med Res 135(3):341–345

    PubMed  Google Scholar 

  • Mandal S, Mandal M, Pal NK, Halder PK, Basu PS (2002) R-factor in Proteus vulgaris from ulcerative disease of fish Channa punctatus. Indian J Exp Biol 40(5):614–616

    CAS  PubMed  Google Scholar 

  • Marine Products Export Development Authority, Network of Aquaculture Centres in Asia-Pacific (2003) Shrimp Health Management Extension Manual. MPEDA house, Cochin, India. pp 23

  • Ministry of Agriculture and Fisheries Bureau of China (2011) China Fisheries Statistical Yearbook. China Agriculture Press, Beijing, China. pp28

  • Orozova P, Sirakov I, Petkov I, Crumlish M, Austin B (2012) Recovery of Aeromonas hydrophila associated with bacteraemia in captive snakes. FEMS Microbiol Lett 334(1):22–26

    Article  CAS  PubMed  Google Scholar 

  • Qi Z, Zhang X, Boon N, Bossier P (2009) Probiotics in aquaculture of China—Current state, problems and prospect. Aquaculture 290:15–21

    Article  Google Scholar 

  • Rajinikanth T, Ramasamy P, Ravi V (2010) Efficacy of probiotics, growth promotors and disinfectants in shrimp grow out farms. World J Fish Mar Sci 2(3):208–215

    CAS  Google Scholar 

  • Robertson PAW, Calderon J, Carrera L, Stark JR, Zherdmant M, Austin B (1998) Experimental Vibrio harveyi infections in Penaeus vannamei larvae. Dis Aquat Organ 32:151–155

    Article  Google Scholar 

  • Rózalski A, Sidorczyk Z, Kotełko K (1997) Potential virulence factors of Proteus bacilli. Microbiol Mol Biol Rev 61(1):65–89

    PubMed Central  PubMed  Google Scholar 

  • Rózalski A, Kwil I, Torzewska A, Baranowska M, Staczek P (2007) Proteus bacilli: features and virulence factors. Postepy Hig Med Dosw 61:204–219

    Google Scholar 

  • Shu XH, Xiao KY, Jin XL, Chen KY, Huang ZJ (1997) Studies on the pathogenic bacteria of the rotten-skin disease of bullfrog. J Fish China 21(suppl):71–76

    Google Scholar 

  • Snyder AR, Williams HN, Baer ML, Walker KE, Stine OS (2002) 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int J Syst Evol Microbiol 52:2089–2094

    Article  CAS  PubMed  Google Scholar 

  • Stock I (2003) Natural antibiotic susceptibility of Proteus spp., with special reference to P. mirabilis and P. penneri strains. J Chemother 15(1):12–26

    Article  CAS  PubMed  Google Scholar 

  • Stolp H, Starr MP (1963) Bdellovibrio bacteriovorus gen. et sp. n., a predatory, ectoparasitic and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29:217–248

    Article  CAS  PubMed  Google Scholar 

  • Wakida-Kusunoki AT, Amador-del Angel LE, Alejandro PC, Brahms CQ (2011) Presence of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) in the Southern Gulf of Mexico. Aquat Invasions 6(Suppl):S139–S142

    Article  Google Scholar 

  • Wang G, Wang Y (1998) Pathology of the caverned disease in soft-shelled turtle (Trionyx sinensis). Acta Univ. Agric 26(4):82–86 Boreali-occidentalis

    CAS  Google Scholar 

  • Wang L, Chen Y, Huang H, Huang Z, Chen H, Shao Z (2013) Isolation and identification of Vibrio campbellii as a bacterial pathogen for luminous vibriosis of Litopenaeus vannamei. Aquac Res. doi:10.1111/are.12191

    Google Scholar 

  • Wen C, Lai X, Xue M, Huang Y, Li H, Zhou S (2009) Molecular typing and identification of Bdellovibrio-and-like organisms isolated from seawater shrimp ponds and adjacent coastal waters. J Appl Microbiol 4:1154–1162

    Article  Google Scholar 

  • Xu B, Ji WH, Xu H (1992) Proteus vulgaris: a new pathogen in Penaeus orientalis. J Fish China 16(2):130–136

    Google Scholar 

  • Xu Q, Li J, Liu Q, Wang Q (2007) Effects of Bdellovibrio bacteriovorus and Rhodotorula glutinis on growth and non-specific immune competence of Fenneropenaeus chinensis. Mar Fish Res 28(5):42–47

    CAS  Google Scholar 

  • Yair S, Yaacov D, Susan K, Jurkevitch E (2003) Small eats big: ecology and diversity of Bdellovibrio and like organisms, and their dynamics in predator-prey interactions. Agronomie 23:433–439

    Article  Google Scholar 

  • Zhang Q, Xiong Q, Xiao L, Yang H, Yang X (2005) A pathogen isolated from skin-ulcer Pseudosciaena crocea-Proteus mirabilis ZXS02 strain. J Fish China 29(6):824–830

    CAS  Google Scholar 

  • Zhang X, Chen C, Yan B, Fang H, Qin G, Xu J (2009) Phenotypic and molecular characterization of pathogenic Vibrio parahaemolyticus isolated from Penaeus vannamei. Oceanologia et Limnologia Sini 5:654–662

    Google Scholar 

  • Zheng T, Kong L, Zhu N (2011) Epidemiology and control strategy of red body disease of Penaeus vannamei in Zhejiang, China. Sci Fish Farm 12:48–49

    Google Scholar 

  • Zhou Y, Zhang B, Chen X, Qian J (2003) Preliminary studies on the red body disease in Penaeus vannamei. Mar Sci 27(5):61–65

    Google Scholar 

  • Zhou Q, Li K, Xie J, Liu B (2009) Role and functions of beneficial microorganisms in sustainable aquaculture. Bioresour Technol 100:3780–3786

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Fang W, Yang X, Zhou S, Hu L, Li X, Qi X, Su H, Xie L (2012) A nonluminescent and highly virulent Vibrio harveyi strain is associated with “bacterial white tail disease” of Litopenaeus vannamei Shrimp. PLoS ONE 7(2):e29961

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work has been financially supported by the Shanghai University Laboratory Technical Team Construction Program, Shangxi Science and Technology Attack Program (No. 20120311025-4), and Jiangsu Agricultural Science and Technology Support Program (No. BE2013366).

Author information

Authors and Affiliations

  1. Key Laboratory of Freshwater Fishery Germplasm Resources, Ministry of Agriculture of P. R. China, Shanghai Engineering Research Center of Aquaculture, Shanghai University Knowledge Service Platform, Shanghai Ocean University Aquatic Animal Breeding Center (ZF1206), National Pathogen Collection Center for Aquatic Animals, Shanghai Ocean University, Shanghai, 201306, People’s Republic of China

    Haipeng Cao, Shan He, Liqun Lu & Xianle Yang

  2. Marine and Fisheries Research Institute of Lianyungang, Lianyungang, 222044, Jiangsu, People’s Republic of China

    Baiyao Chen

Authors
  1. Haipeng Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shan He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liqun Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianle Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Baiyao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Haipeng Cao or Baiyao Chen.

Additional information

Haipeng Cao and Shan He are contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 324 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cao, H., He, S., Lu, L. et al. Identification of a Proteus penneri isolate as the causal agent of red body disease of the cultured white shrimp Penaeus vannamei and its control with Bdellovibrio bacteriovorus . Antonie van Leeuwenhoek 105, 423–430 (2014). https://doi.org/10.1007/s10482-013-0079-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-013-0079-y

Keywords

Search

Navigation