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White spot syndrome virus (WSSV) disturbs the intestinal microbiota of shrimp (Penaeus vannamei) reared in biofloc and clear seawater

Applied Microbiology and Biotechnology volume 104, pages 8007–8023 (2020)Cite this article

Abstract

White spot syndrome virus (WSSV) is one of the most virulent pathogens afflicting shrimp farming. Understanding its influence on shrimp intestinal microbiota is paramount for the advancement of aquaculture, since gut dysbiosis can negatively impact shrimp development, physiology, and immunological response. Thereupon, the data presented herein assesses the influence of WSSV infection and different rearing systems on the intestinal microbiota of Penaeus vannamei. Our study aimed to describe and correlate the composition of shrimp (Penaeus vannamei) gut microbiota, when reared in biofloc and clear seawater, before and (48 h) after WSSV experimental infection. Shrimp were kept in two different systems (biofloc and clear seawater) and experimentally infected with WSSV. Intestine and water samples were characterized by 16S rRNA gene sequencing, before and after viral infection. We observed (i) WSSV induced higher mortality among shrimp reared in biofloc; (ii) WSSV led to a loss of intestinal microbiota heterogeneity, at the genus level, in shrimp kept in clear seawater; (iii) there was a prevalence of Cetobacterium and Bacillus in the intestine of shrimp from both systems; (iv) WSSV did not cause significant changes in intestinal microbiota diversity or richness; (v) regardless of the type of system and time of infection, intestinal microbiota was dissimilar to that of the surrounding water, despite being influenced by the type of system. Therefore, WSSV infection leads to punctual dysbiotic changes in shrimp microbiota, although the virus is sufficiently virulent to cause high mortalities even in well-managed systems, such as a balanced experimental biofloc system.

Key points

• WSSV infection leads to a perturbed gut microbiota in shrimp.

• WSSV infection greater impacts microbiota of shrimp reared in CSW than those in BFT.

• WSSV infection caused higher mortality levels in shrimp reared in BFT than in CSW.

• Rearing system influences shrimp gut microbiota composition.

Graphical abstract

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Data availability

The authors disclose that all data supporting the findings presented in the manuscript are available within the manuscript and supplemental material.

References

  • Ahmad I, Rani AB, Verma AK, Maqsood M (2017) Biofloc technology: an emerging avenue in aquatic animal healthcare and nutrition. Aquacul Int 25(3):1215–1226

    CAS  Google Scholar 

  • Amoah K, Huang QC, Tan BP, Zhang S, Chi SY, Yang QH, Liu HY, Dong XH (2019) Dietary supplementation of probiotic Bacillus coagulans ATCC 7050, improves the growth performance, intestinal morphology, microflora, immune response and disease confrontation of Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immun 87:796–808

    CAS  Google Scholar 

  • Australian Government. Department of Agriculture and Water Resources (2017) Report into the cause of white spot syndrome virus outbreak in the Logan River area of Queensland – December 2016. Commonwealth, Canberra

    Google Scholar 

  • Avnimelech Y (2014) Intensive production of shrimp. In: Alday-Sanz V (ed) The shrimp book. Nottingham University Press, Nottingham, pp 233–246

    Google Scholar 

  • Becker MH, Brucker RM, Schwantes CR, Harris RN, Minbiole KP (2009) The bacterially produced metabolite violacein is associated with survival of amphibians infected with a lethal fungus. Appl Environ Microbiol 75(21):6635–6638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cardona E, Gueguen Y, Magré K, Lorgeoux B, Piquemal D, Pierrat F, Noguier F, Saulnier D (2016) Bacterial community characterization of water and intestine of the shrimp Litopenaeus stylirostris in a biofloc system. BMC Microbiol 16(1):157–165

    PubMed  PubMed Central  Google Scholar 

  • Castex M, Daniels C, Chim L (2014) Probiotic applications in Crustaceans. In: Merrifield D, Ringø E (eds) Aquaculture Nutrition: Gut Health, Probiotics and Prebiotics. Wiley, West Sussex, pp 290–327

    Google Scholar 

  • Chen WY, Ng TH, Wu JH, Chen JW, Wang HC (2017) Microbiome dynamics in a shrimp grow-out tank with possible outbreak of acute hepatopancreatic necrosis disease. Sci Rep 7(1):9395

    PubMed  PubMed Central  Google Scholar 

  • Cheung MK, Yip HY, Nong W, Law PTW, Chu KH, Kwan HS, Hui JHL (2015) Rapid change of microbiota diversity in the gut but not the hepatopancreas during gonadal development of the new shrimp model Neocaridina denticulata. Mar Biotechnol 17(6):811–819

    CAS  PubMed  Google Scholar 

  • Cornejo-Granados F, Lopez-Zavala AA, Gallardo-Becerra L, Mendoza-Vargas A, Sánchez F, Vichido R, Ochoa-Leyva A (2017) Microbiome of Pacific whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Sci Rep 7(1):11783

  • Cornejo-Granados F, Gallardo-Becerra L, Leonardo-Reza M, Ochoa-Romo JP, Ochoa-Leyva A (2018) A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota. PeerJ 6:e5382

    PubMed  PubMed Central  Google Scholar 

  • Crab R, Lambert A, Defoirdt T, Bossier P, Verstraete W (2010) The application of bioflocs technology to protect brine shrimp (Artemia franciscana) from pathogenic Vibrio harveyi. J Appl Microbiol 109(5):1643–1649

    CAS  PubMed  Google Scholar 

  • Crab R, Defoirdt T, Bossier P, Verstraete W (2012) Biofloc technology in aquaculture: beneficial effects and future challenges. Aquac 356:351–356

    Google Scholar 

  • Deng Y, Xu X, Yin X, Lu H, Chen G, Yu J, Ruan Y (2019) Effect of stock density on the microbial community in biofloc water and Pacific white shrimp (Litopenaeus vannamei) gut microbiota. Appl Microbiol Biot 103(10):4241–4252

    CAS  Google Scholar 

  • Ding ZF, Cao MJ, Zhu XS, Xu GH, Wang RL (2017) Changes in the gut microbiome of the Chinese mitten crab (Eriocheir sinensis) in response to white spot syndrome virus (WSSV) infection. J Fish Dis 40(11):1561–1571

  • Emerenciano MGC, Martínzes-Córdova LR, Martínez-Porchas M, Miranda-Baeza A (2017) Biofloc Technology (BFT): A tool for water quality management in aquaculture. In: Tutu H (ed) Water Quality. In tech, London, pp 91–109.

  • Fan L, Wang Z, Chen M, Qu Y, Li J, Zhou A, Xie S, Zeng F, Zou J (2019a) Microbiota comparison of Pacific white shrimp intestine and sediment at freshwater and marine cultured environment. Sci Total Environ 657:1194–1204

    CAS  PubMed  Google Scholar 

  • Fan J, Chen L, Mai G, Zhang H, Yang J, Deng D, Ma Y (2019b) Dynamics of the gut microbiota in developmental stages of Litopenaeus vannamei reveal its association with body weight. Sci Rep 9(1):1–10

    Google Scholar 

  • Finegold SM, Vaisanen ML, Molitoris DR, Tomzynski TJ, Song Y, Liu C, Collins MD, Lawson PA (2003) Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. Syst Appl Microbiol 26(2):177–181

    PubMed  Google Scholar 

  • Flegel TW (2019) A future vision for disease control in shrimp aquaculture. J World Aquacult Soc 50(2):249–266

    Google Scholar 

  • Flegel TW, Sritunyalucksana K (2011) Shrimp molecular responses to viral pathogens. Mar Biotechnol 13(4):587–607

    CAS  PubMed  Google Scholar 

  • Gajardo K, Rodiles A, Kortner TM, Krogdahl Å, Bakke AM, Merrifield DL, Sørum H (2016) A high-resolution map of the gut microbiota in Atlantic salmon (Salmo salar): A basis for comparative gut microbial research. Sci Rep 6:30893

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao S, Pan L, Huang F, Song M, Tian C, Zhang M (2019) Metagenomic insights into the structure and function of intestinal microbiota of the farmed Pacific white shrimp (Litopenaeus vannamei). Aquac 499:109–118

    CAS  Google Scholar 

  • Gerdts G, Brandt P, Kreisel K, Boersma M, Schoo KL, Wichels A (2013) The microbiome of North Sea copepods. Helgol Mar Res 67(4):757

    Google Scholar 

  • Godoy-Vitorino F, Rodriguez-Hilario A, Alves AL, Gonçalves F, Cabrera-Colon B, Mesquita CS, Soares-Castro P, Ferreira M, Marçalo A, Vingada J, Eira C, Santos PM (2017) The microbiome of a striped dolphin (Stenella coeruleoalba) stranded in Portugal. Res Microbiol 168(1):85–93

    PubMed  Google Scholar 

  • Griffith DRW (2014) White spot and Taura syndrome virus: disease as drivers in the shrimp farming industry. In: Alday-Sanz V (ed) The shrimp book. Nottingham University Press, Nottingham, pp 429–441

    Google Scholar 

  • Hao K, Liu JY, Ling F, Liu XL, Lu L, Xia L, Wang GX (2014) Effects of dietary administration of Shewanella haliotis D4, Bacillus cereus D7 and Aeromonas bivalvium D15, single or combined, on the growth, innate immunity and disease resistance of shrimp, Litopenaeus vannamei. Aquac 428:141–149

    Google Scholar 

  • Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16(1):169

    PubMed  PubMed Central  Google Scholar 

  • Huang Z, Li X, Wang L, Shao Z (2016) Changes in the intestinal bacterial community during the growth of white shrimp, Litopenaeus vannamei. Aquac Res 47(6):1737–1746

    Google Scholar 

  • Jaramillo-Torres A, Rawling M, Rodiles A, Mikalsen HE, Johansen LH, Tinsley J, Forberg T, Aasum E, Castex M, Merrifield DL (2019) Influence of dietary supplementation of probiotic Pediococcus acidilactici MA18/5 M during the transition from freshwater to seawater on intestinal health and microbiota of Atlantic salmon (Salmo salar L.). Front Microbiol 10:2243

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

    Google Scholar 

  • Karst SM (2016) The influence of commensal bacteria on infection with enteric viruses. Nat Rev Microbiol 14(4):197–204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karunasagar I, Karunasagar I, Alday-Sanz V (2014) Immunostimulants, probiotics and phage therapy: alternatives to antibiotics. In: Alday-Sanz V (ed) The shrimp book. Nottingham University Press, Nottingham, p 695711

    Google Scholar 

  • Khanjani MH, Sharifinia M (2020) Biofloc technology as a promising tool to improve aquaculture production. Rev Aquacult. https://doi.org/10.1111/raq.12412

  • Kirchman DL (2012) Community structure of microbes in natural environments. In: Kirchman DL (ed) Process in Microbial Ecology. Oxford University Press, Oxford, pp 157–176

    Google Scholar 

  • Lafferty KD, Harvell CD, Conrad JM, Friedman CS, Kent ML, Kuris AM, Powel EN, Rondeau D, Saksida SM (2015) Infectious diseases affect marine fisheries and aquaculture economics. Annu Rev Mar Sci 7:471–496

    Google Scholar 

  • Lage OM, Bondoso J (2012) Bringing Planctomycetes into pure culture. Front Microbiol 3:405

    PubMed  PubMed Central  Google Scholar 

  • Lakshmi B, Viswanath B, Sai Gopal DVR (2013) Probiotics as antiviral agents in shrimp aquaculture. J Pathog 2013. https://doi.org/10.1155/2013/424123

  • Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6(10):776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li E, Xu C, Wang X, Wang S, Zhao Q, Zhang M, Qin JG, Chen L (2018) Gut microbiota and its modulation for healthy farming of Pacific white shrimp Litopenaeus vannamei. Rev Fish Sci Aquac 26(3):381–399

    Google Scholar 

  • Liang Y, Xu ML, Wang XW, Gao XX, Cheng JJ, Li C, Huang J (2015) ATP synthesis is active on the cell surface of the shrimp Litopenaeus vannamei and is suppressed by WSSV infection. Virol J 12(1):49

    PubMed  PubMed Central  Google Scholar 

  • Lightner DV, Redman RM, Pantoja CR, Tang KFJ, Noble BL, Schofield P, Mohney LL, Nunan LM, Navarro SA (2012) Historic emergence, impact and current status of shrimp pathogens in the Americas. J Invertebr Pathol 110(2):174–183

    CAS  PubMed  Google Scholar 

  • Lin YC, Chen JC, Man SNC, Morni WZW, Suhaili ASN, Cheng SY, Hsu CH (2012) Modulation of innate immunity and gene expressions in white shrimp Litopenaeus vannamei following long-term starvation and re-feeding. Results Immunol 2:148–156

    PubMed  PubMed Central  Google Scholar 

  • Liu H, Li H, Wei H, Zhu X, Han D, Jin J, Yang Y, Xie S (2019) Biofloc formation improves water quality and fish yield in a freshwater pond aquaculture system. Aquac 506:256–269

    CAS  Google Scholar 

  • Madani NSH, Adorian TJ, Ghafari Farsani H, Hoseinifar SH (2018) The effects of dietary probiotic Bacilli (Bacillus subtilis and Bacillus licheniformis) on growth performance, feed efficiency, body composition and immune parameters of whiteleg shrimp (Litopenaeus vannamei) postlarvae. Aquac Res 49(5):1926–1933

    Google Scholar 

  • Mark V (2012) Epigenetics: Reading the second genomic code. Nature 91:143–147

    Google Scholar 

  • Mazón-Suástegui JM, Salas-Leiva JS, Medina-Marrero R, Medina-García R, García-Bernal M (2020) Effect of Streptomyces probiotics on the gut microbiota of Litopenaeus vannamei challenged with Vibrio parahaemolyticus. Microbiologyopen 9(2):e967

  • Merrifield D, Ringo E (2014) Aquaculture nutrition: gut health, probiotics and prebiotics. Wiley, West Sussex

    Google Scholar 

  • Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290(5494):1166–1168

    CAS  PubMed  Google Scholar 

  • Mukherjee A, Rodiles A, Merrifield DL, Chandra G, Ghosh K (2020) Exploring intestinal microbiome composition in three Indian major carps under polyculture system: a high-throughput sequencing based approach. Aquac 524:735206

  • Müller IC (2009). Genes diferencialmente expressos em camarões de cultivo Litopenaeus vannamei infectados pelo vírus da Síndrome da Mancha Branca e genotipagem de isolados geográficos brasileiros do vírus. Ph.D. thesis. Federal University of Santa Catarina.

  • Muller IC, Andrade TP, Tang-Nelson KF, Marques MR, Lightner DV (2010) Genotyping of white spot syndrome virus (WSSV) geographical isolates from Brazil and comparison to other isolates from the Americas. Dis Aquat Org 88(2):91–98

    CAS  PubMed  Google Scholar 

  • Oetama VS, Hennersdorf P, Abdul-Aziz MA, Mrotzek G, Haryanti H, Saluz HP (2016) Microbiome analysis and detection of pathogenic bacteria of Penaeus monodon from Jakarta Bay and Bali. Mar Pollut Bull 110(2):718–725

    CAS  PubMed  Google Scholar 

  • OIE (Office International des Epizooties) (2016) Disease timelines. [Online]. Available at: http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/Diseasetimelines. Accessed 24 May 2017

  • Peraza-Gómez V, Luna-González A, Campa-Córdova ÁI, López-Meyer M, Fierro-Coronado JA, Álvarez-Ruiz P (2009) Probiotic microorganisms and antiviral plants reduce mortality and prevalence of WSSV in shrimp (Litopenaeus vannamei) cultured under laboratory conditions. Aquac Res 40(13):1481–1489

    Google Scholar 

  • Pereira GV, Pereira SA, Soares A, Mouriño JLP, Merrifield D (2019) Autochthonous probiotic bacteria modulate intestinal microbiota of Pirarucu, Arapaima gigas. J World Aquacult Soc 50(6):1152–1167

    Google Scholar 

  • Pilotto M, Goncalves A, Vieira F, Seifert W, Bachère E, Rosa R, Perazzolo L (2018) Exploring the impact of the biofloc rearing system and an oral WSSV challenge on the intestinal bacteriome of Litopenaeus vannamei. Microorganisms 6(3):83

  • Prior S, Browdy CL, Shepard EF, Laramore R, Parnell PG (2003) Controlled bioassay systems for determination of lethal infective doses of tissue homogenates containing Taura syndrome or white spot syndrome virus. Dis Aquat Org 54(2):89–96

    PubMed  Google Scholar 

  • Qi XZ, Tu X, Zha JW, Huang AG, Wang GX, Ling F (2019) Immunosuppression-induced alterations in fish gut microbiota may increase the susceptibility to pathogens. Fish Shellfish Immun 88:540–545

    CAS  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(3):e91853

  • Rungrassamee W, Klanchui A, Maibunkaew S, Karoonuthaisiri N (2016) Bacterial dynamics in intestines of the black tiger shrimp and the Pacific white shrimp during Vibrio harveyi exposure. J Invertebr Pathol 133:12–19

    CAS  PubMed  Google Scholar 

  • Sajali USBA, Atkinson NL, Desbois AP, Little DC, Murray FJ, Shinn AP (2019) Prophylactic properties of biofloc-or Nile tilapia-conditioned water against Vibrio parahaemolyticus infection of whiteleg shrimp (Penaeus vannamei). Aquac 498:496–502

    Google Scholar 

  • Sajeevan TP, Philip R, Singh IB (2009) Dose/frequency: a critical factor in the administration of glucan as immunostimulant to Indian white shrimp Fenneropenaeus indicus. Aquac 287(4):248–252

    CAS  Google Scholar 

  • Sandeepa GM, Ammani K (2017) Immunological and Antioxidant Response of Litopenaeus vannamei fed with Lactobacillus species under WSSV challenge. Curr Trends Biotechnol Pharm 11:1

    Google Scholar 

  • Schlesner H (1994) The development of media suitable for the microorganisms morphologically resembling Planctomyces spp., Pirellula spp. and other Planctomycetales from various aquatic habitats using dilute media. Syst Appl Microbiol 17(1):135–145

    Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60

    PubMed  PubMed Central  Google Scholar 

  • Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C (2012) Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 9(8):811

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shekhar MS, Azad IS, Ravichandran P (2006) Comparison of dot blot and PCR diagnostic techniques for detection of white spot syndrome virus in different tissues of Penaeus monodon. Aquac 261(4):1122–1127

    CAS  Google Scholar 

  • Silva KR, Wasielesky W Jr, Abreu PC (2013) Nitrogen and phosphorus dynamics in the biofloc production of the pacific white shrimp, Litopenaeus vannamei. J World Aquacult Soc 44(1):30–41

    Google Scholar 

  • Soonthornchai W, Chaiyapechara S, Jarayabh P, Söderhäll K, Jiravanichpaisal P (2015) Interaction of Vibrio spp. with the inner surface of the digestive tract of Penaeus monodon. PloS one 10(8):e0135783

  • Souza Valente C, Ortiz KO, Depperschmidt R, de Medeiros Fraga AP, do Nascimento Vieira F, Marques MRF (2020) Transcription of defense related genes in Pacific white shrimp, Litopenaeus vannamei, kept in biofloc and in clear seawater and challenged with the white spot syndrome virus. Aquacul Int 28:293–307

    Google Scholar 

  • Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics. J Appl Microbiol 123(1):2–17

    CAS  PubMed  Google Scholar 

  • Tepaamorndech S, Chantarasakha K, Kingcha Y, Chaiyapechara S, Phromson M, Sriariyanun M, Kirschke CP, Huang L, Visessanguan W (2019) Effects of Bacillus aryabhattai TBRC8450 on vibriosis resistance and immune enhancement in Pacific white shrimp, Litopenaeus vannamei. Fish Shellfish Immun 86:4–13

    CAS  Google Scholar 

  • Thammasorn T, Jitrakorn S, Charoonnart P, Sirimanakul S, Rattanarojpong T, Chaturongakul S, Saksmerprome V (2017) Probiotic bacteria (Lactobacillus plantarum) expressing specific double-stranded RNA and its potential for controlling shrimp viral and bacterial diseases. Aquacul Int 25(5):1679–1692

    CAS  Google Scholar 

  • Tsuchiya C, Sakata T, Sugita H (2008) Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol 46:43–48

    CAS  PubMed  Google Scholar 

  • Tzeng TD, Pao YY, Chen PC, Weng FCH, Jean WD, Wang D (2015) Effects of host phylogeny and habitats on gut microbiomes of oriental river prawn (Macrobrachium nipponense). PloS one 10(7):e0132860

  • Valentim-Neto PA, Fraga AP, Marques MR (2014) Differential expression of proteins in the gills of Litopenaeus vannamei infected with white spot syndrome virus. Aquacul Int 22(5):1605–1620

    CAS  Google Scholar 

  • Virgin S (2007) Pathogenesis of Viral Infection. In: Knipe DM, Howley PM (eds) Fields Virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 328–389

    Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Huang Y, Xu K, Zhang X, Sun H, Fan L, Yan M (2019) White spot syndrome virus (WSSV) infection impacts intestinal microbiota composition and function in Litopenaeus vannamei. Fish Shellfish Immun 84:130–137

    Google Scholar 

  • Wei J, Yu N, Tian W, Zhang F, Wu Q, Li E, Zhang M, Du Z, Qin J, Chen L (2014) Dietary vitamin B12 requirement and its effect on non-specific immunity and disease resistance in juvenile Chinese mitten crab Eriocheir sinensis. Aquac 434:179–183

    CAS  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 Biot 99(16):6911–6919

    CAS  Google Scholar 

  • Xiong J, Dai W, Zhu J, Liu K, Dong C, Qiu Q (2017) The underlying ecological processes of gut microbiota among cohabitating retarded, overgrown and normal shrimp. Microb Ecol 73(4):988–999

    PubMed  Google Scholar 

  • Xiong J, Dai W, Qiu Q, Zhu J, Yang W, Li C (2018) Response of host–bacterial colonization in shrimp to developmental stage, environment and disease. Mol Ecol 27(18):3686–3699

    PubMed  Google Scholar 

  • Zhu B, Wang X, Li L (2010) Human gut microbiome: the second genome of human body. Protein Cell 1:718–724

    PubMed  PubMed Central  Google Scholar 

  • Zoqratt MZHM, Eng WWH, Thai BT, Austin CM, Gan HM (2018) Microbiome analysis of Pacific white shrimp gut and rearing water from Malaysia and Vietnam: implications for aquaculture research and management. PeerJ 6:e5826. https://doi.org/10.7717/peerj.5826

    CAS  Article  Google Scholar 

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Acknowledgments

We thank the staff from the Marine Shrimp Laboratory (UFSC, Brazil) for their daily assistance during the experiment and staff from the School of Biological & Marine Science (University of Plymouth, UK) for their support on molecular analysis.

Funding

This work was supported by the Brazilian official funding agency, The National Council for Scientific and Technological Development – CNPq, Proc 407211/2012-8; Proc 311099/2012-0.

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Author notes

  1. Ana Rodiles

    Present address: Lallemand Animal Nutrition, Lallemand SAS, 31702, Blagnac, France

Affiliations

  1. Laboratory of Biomarkers of Aquatic Contamination and Immunochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianopolis, SC, Brazil

    Cecília de Souza Valente & Maria Risoleta Freire Marques

  2. School of Biological & Marine Sciences, Faculty of Science & Engineering, University of Plymouth, Plymouth, UK

    Ana Rodiles & Daniel Lee Merrifield

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  1. Cecília de Souza Valente
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Contributions

CSV and MRFM conceived and designed the research. CSV and MRFM conducted experiments. MRFM and DM provided funding. CSV, AR, MRFM, and DM analyzed the data. The first draft of the manuscript was written by CSV and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Cecília de Souza Valente.

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CSV received a CAPES (Coordination of Superior Level Staff Improvement) scholarship from the Aquaculture Graduate Program at UFSC. MRFM is the recipient of a CNPq (National Council for Scientific and Technological Development) productivity research grant. AR and DLM declare no conflict of interest. This work was part of the first author’s doctoral studies.

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de Souza Valente, C., Rodiles, A., Freire Marques, M.R. et al. White spot syndrome virus (WSSV) disturbs the intestinal microbiota of shrimp (Penaeus vannamei) reared in biofloc and clear seawater. Appl Microbiol Biotechnol 104, 8007–8023 (2020). https://doi.org/10.1007/s00253-020-10816-4

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Keywords

  • 16S rRNA gene
  • microbiome
  • NGS
  • Pacific white shrimp