Skip to main content

Intestinal bacterial signatures of white feces syndrome in shrimp

Applied Microbiology and Biotechnology volume 102, pages 3701–3709 (2018)Cite this article

Abstract

Increasing evidence suggests that the intestinal microbiota is closely correlated with the host’s health status. Thus, a serious disturbance that disrupts the stability of the intestinal microecosystem could cause host disease. Shrimps are one of the most important products among fishery trading commodities. However, digestive system diseases, such as white feces syndrome (WFS), frequently occur in shrimp culture and have led to enormous economic losses across the world. The WFS occurrences are unclear. Here, we compared intestinal bacterial communities of WFS shrimp and healthy shrimp. Intestinal bacterial communities of WFS shrimp exhibited less diversity but were more heterogeneous than those of healthy shrimp. The intestinal bacterial communities were significantly different between WFS shrimp and healthy shrimp; compared with healthy shrimp, in WFS shrimp, Candidatus Bacilloplasma and Phascolarctobacterium were overrepresented, whereas Paracoccus and Lactococcus were underrepresented. PICRUSt functional predictions indicated that the relative abundances of genes involved in energy metabolism and genetic information processing were significantly greater in WFS shrimp. Collectively, we found that the composition and predicted functions of the intestinal bacterial community were markedly shifted by WFS. Significant increases in Candidatus Bacilloplasma and Phascolarctobacterium and decreases in Paracoccus and Lactococcus may contribute to WFS in shrimp.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Adel M, Sayed AF, Yeganeh S, Dadar M, Giri S (2017) Effect of potential probiotic Lactococcus lactis subsp. lactis on growth performance, intestinal microbiota, digestive enzyme activities, and disease resistance of Litopenaeus vannamei. Probiotics Antimicro 9:150–156

    Article  CAS  Google Scholar 

  • Cai H, Jiang H, Krumholz LR, Yang Z (2014) Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS One 9:e102879

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi MY, Stevens AM, Smith SA, Taylor DP, Kuhn DD (2016) Strain and dose infectivity of Vibrio parahaemolyticus: the causative agent of early mortality syndrome in shrimp. Aquac Res 48:3719–3727

    Article  Google Scholar 

  • Clarke SF, Murphy EF, O,Sullivan O, Lucey AJ, Humphreys M, Hogan A (2014) Exercise and associated dietary extremes impact on gut microbial diversity. Gut 63: 1913–1920

  • Clemente JC, Ursell LK, Parfrey LW, Knight B (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai W, Yu W, Zhang J, Zhu J, Tao Z, Xiong J (2017) The gut eukaryotic microbiota influences the growth performance among cohabitating shrimp. Appl Microbiol Biotechnol 101:6447–6457

    Article  CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf 5:1–31

    Article  Google Scholar 

  • FAO (2015) Fishery and aquaculture statistics. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6:121–131

    Article  CAS  PubMed  Google Scholar 

  • Hao Y, Wu S, Xiong F, Tran NT, Jakovlic I, Zou H, Li WX, Wang GT (2017) Succession and fermentation products of grass carp (Ctenopharyngodon idellus) hindgut microbiota in response to an extreme dietary shift. Front Microbiol 8:1585

    Article  PubMed  PubMed Central  Google Scholar 

  • Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115–1118

    Article  CAS  PubMed  Google Scholar 

  • Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, Malinen E, Apajalahti J, Palva A (2007) The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133:24–33

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi Y, Hayatsu M, Hosokawa T, Nagayama A, Tago K, Fukatsu T (2012) Symbiont-mediated insecticide resistance. Proc Natl Acad Sci U S A 109:8618–8622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostanjsek R, Strus J, Avgustin G (2007) “Candidatus Bacilloplasma,” a novel lineage of mollicutes associated with the hindgut wall of the terrestrial isopod Porcellio scaber (Crustacea: isopoda). Appl Environ Microbiol 73:5566–5573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG, Huttenhower G (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebel L, Mungkung R, Gheemala SH, Lebel P (2010) Innovation cycles, niches and sustainability in the shrimp aquaculture industry in Thailand. Environ Sci Pol 13:291–302

    Article  Google Scholar 

  • Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb Ecol 69:25–36

    Article  CAS  PubMed  Google Scholar 

  • Li T, Long M, Ji C, Shen ZX, Gatesoupe FJ, Zhang XJ, Zhang Q, Zhang L, Zhao Y, Liu X, Li A (2016a) Alterations of the gut microbiome of largemouth bronze gudgeon (Coreius guichenoti) suffering from furunculosis. Sci Rep 6:30606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Xie W, Li Q (2016b) Characterisation of the bacterial community structures in the intestine of Lampetra morii. Antonie Van Leeuwenhoek 109:979–986

    Article  CAS  PubMed  Google Scholar 

  • Li T, Li H, Gatesoupe FJ, She R, Lin Q, Yan X, Li J, Li X (2017) Bacterial signatures of “red-operculum” disease in the gut of crucian carp (Carassius auratus). Microb Ecol 74:510–521. https://doi.org/10.1007/s00248-017-0967-1

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, Timmis KN, Schreiber S (2004) Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 53:685–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oxley APA, Shipton W, Owens L, McKay D (2002) Microbial flora from the gut of the wild and cultured banana prawn, Penaeus merguiensis. J Appl Microbiol 93:214–223

    Article  CAS  PubMed  Google Scholar 

  • Panadiyan P, Balaraman D, Thirunavukkarasu B, George EGJ, Subaramaniyan K, Manikkam S, Sadayappan B (2013) Probiotics in aquaculture. Drug Invention Today 5:55–59

    Article  Google Scholar 

  • Perez T, Balcazar JL, Zarzuela IR, Halaihel N, Vendrell D, Blas I, Muzquiz JL (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360

    Article  CAS  PubMed  Google Scholar 

  • Qin N, Yang F, Li A, Prifti E, Chen Y, Shao L (2014) Alterations of the human gutmicrobiome in liver cirrhosis. Nature 513:59–67

    Article  CAS  PubMed  Google Scholar 

  • Ramirez C, Romero J (2017) Fine flounder (Paralichthys adspersus) microbiome showed important differences between wild and reared specimens. Front Microbiol 8:271

    PubMed  PubMed Central  Google Scholar 

  • Rawls JF, Samuel BS, Gordon JI (2004) Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proc Natl Acad Sci U S A 101:4596–4601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rungrassamee W, Klanchui A, Maibunkaew S, Chaiyapechara S, Jiravanichpaisal P, Karoonuthaisiri N (2013) Bacterial population in intestines of the black tiger shrimp (Penaeus monodon) under different growth stages. PLoS One 8:e60802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rungrassamee W, Klanchui A, Maibunkaew S, Chaiyapechara S, Jiravanichpaisal P, Karoonuthaisiri N (2014) Characterization of intestinal bacteria in wild and domesticated adult black tiger shrimp (Penaeus monodon). PLoS One 9:e91853

    Article  PubMed  PubMed Central  Google Scholar 

  • Scher JU, Ubeda G, Artacho A, Attur M, Isaac S, Reddy SM (2015) Decreased bacterial diversity characterizes an altered gut microbiota in psoriatic arthritis and resembles dysbiosis of inflammatory bowel disease. Arthritis Rheum 67:128–139

    Article  CAS  Google Scholar 

  • Sekirov I, Russell SL, Antunes LCM, Finlay B (2010) Gut microbiota in health and disease. Physiol Rev 90:859–890

    Article  CAS  PubMed  Google Scholar 

  • Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, Chang EB, Gajewski TF (2015) Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350:1084–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smriga S, Sandin SA, Azam F (2010) Abundance, diversity, and activity of microbial assemblages associated with coral reef fish guts and feces. FEMS Microbiol Ecol 73:31–42

    CAS  PubMed  Google Scholar 

  • Sriurairatana S, Boonyawiwat V, Gangnonngiw W, Laosutthipong C, Hiranchan J, Flegel TW (2014) White feces syndrome of shrimp arises from transformation, sloughing and aggregation of hepatopancreatic microvilli into vermiform bodies superficially resembling gregarines. PLoS One 9(6):e99170

    Article  PubMed  PubMed Central  Google Scholar 

  • Tangprasittipap A, Srisala J, Chouwdee S, Somboon M, Chuchird N, Limsuwan C, Srisuvan T, Flegel TW, Sritunyalucksana K (2013) The microsporidian Enterocytozoon hepatopenaei is not the cause of white feces syndrome in whiteleg shrimp Penaeus (Litopenaeus) vannamei. BMC Vet Res 9:139

    Article  PubMed  PubMed Central  Google Scholar 

  • Walter J, Britton RA, Roos S (2011) Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm. Proc Natl Acad Sci U S A 108:4645–4652

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu S, Wang G, Angert E, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing M, Hou Z, Yuan J, Liu Y, Qiu Y, Liu B (2013) Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot (Scophthalmus maximus). FEMS Microbiol Ecol 86:432–443

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Wang K, Wu J, Qiuqian L, Yang K, Qian Y, Zhang D (2015) Changes in intestinal bacterial communities are closely associated with shrimp disease severity. Appl Microbiol Biotechnol 99:6911–6919

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Dai W, Li C (2016) Advances, challenges, and directions in shrimp disease control: the guidelines from an ecological perspective. Appl Microbiol Biotechnol 100:6947–6954

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Dai W, Zhu J, Liu K, Dong C, Qiu Q (2017a) The underlying ecological processes of gut microbiota among cohabitating retarded, overgrown and normal shrimp. Microb Ecol 73:988–999

    Article  PubMed  Google Scholar 

  • Xiong J, Zhu J, Dai W, Dong C, Qiu Q, Li C (2017b) Integrating gut microbiota immaturity and disease-discriminatory taxa to diagnose the initiation and severity of shrimp disease. Environ Microbiol 19:1490–1501

    Article  PubMed  Google Scholar 

  • Yan Q, Li J, Yu Y, Wang J, He Z, Nostrand JDV, Kempher ML, Wu L, Wang Y, Liao L, Li X, Wu S, Ni J, Wang C, Zhou J (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18:4739–4754

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Guo Z, Xue Z, Sun Z, Zhang M, Wang L (2015) A phylo-functional core of gut microbiota in healthy young Chinese cohorts across lifestyles, geography and ethnicities. ISME J 9:1979–1990

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Li A, Reafey MM, Xu W (2017) High spatial and temporal variations of microbial community along the southern catfish gastrointestinal tract: insights into dynamic food digestion. Front Microbiol 8:1531

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Dai W, Qiu Q, Dong C, Zhang J, Xiong J (2016) Contrasting ecological processes and functional compositions between intestinal bacterial community in healthy and diseased shrimp. Microb Ecol 72:975–985

    Article  PubMed  Google Scholar 

Download references

Funding

This work was financially supported by the China Agriculture Research System (CARS-48), the Guangzhou Science Technology and Innovation Commission Project (201510010071), and the Guangdong Ocean and Fishery Bureau Project (20164200042090023).

Author information

Author notes

  1. Dongwei Hou, Zhijian Huang, and Shenzheng Zeng contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, School of Marine Sciences, Sun Yat-sen University, Guangzhou, 510275, People’s Republic of China

    Dongwei Hou, Zhijian Huang, Shenzheng Zeng, Jian Liu, Dongdong Wei, Xisha Deng & Jianguo He

  2. School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, People’s Republic of China

    Shaoping Weng & Jianguo He

  3. Environmental Microbiomics Research Center and School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou, 510006, People’s Republic of China

    Qingyun Yan

Authors
  1. Dongwei Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhijian Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shenzheng Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dongdong Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xisha Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shaoping Weng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qingyun Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jianguo He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhijian Huang or Jianguo He.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical statement

This article does not contain any studies with human participants by any of the authors. No specific permits were required for the described field studies. No specific permissions were required for access to the artificial pond in Maoming, Guangdong Province, China. The field studies did not involve endangered or protected species. This study was reviewed and approved by the ethics committee of Sun Yat-sen University.

Electronic supplementary material

ESM 1

(PDF 128 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hou, D., Huang, Z., Zeng, S. et al. Intestinal bacterial signatures of white feces syndrome in shrimp. Appl Microbiol Biotechnol 102, 3701–3709 (2018). https://doi.org/10.1007/s00253-018-8855-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-8855-2

Keywords

  • Intestinal microbiota
  • Shrimp
  • Pacific white shrimp
  • White feces syndrome
  • Diversity