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16 S rRNA gene diversity and gut microbial composition of the Indian white shrimp (Penaeus indicus)

Abstract

The endemic Indian white shrimp (Penaeus indicus) is an economically important crustacean species, distributed in the Indo-West Pacific region. Knowledge of its gut microbial composition helps in dietary interventions to ensure improved health and production. Here we analyzed V3-V4 hypervariable regions of the 16 S rRNA gene to examine intestinal microbiota in wild and domesticated farmed P. indicus. The study revealed that Proteobacteria, Fusobacteria, Tenericutes, and Bacteroidetes, were the dominant phyla in both the groups although there were differences in relative abundance. The dominant genera in case of the wild group were Photobacterium (29.5 %) followed by Propionigenium (13.9 %), Hypnocyclicus (13.7 %) and Vibrio (11.1 %); while Vibrio (46.5 %), Catenococcus (14 %), Propionigenium (10.3 %) and Photobacterium (8.7 %) were dominant in the farmed group. The results of the study suggest the role of environment on the relative abundance of gut bacteria. This is the first report characterizing gut microbial diversity in P. indicus, which can be used to understand the role of gut microbiota in health, nutrition, reproduction, and growth.

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Data availability

The raw sequences obtained in this study are available through the NCBI BioProject ID (PRJNA610456).

References

  1. Antwis RE, Edwards KL, Unwin B, Walker SL, Shultz S (2019) Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome 7:27

    PubMed  PubMed Central  Article  Google Scholar 

  2. Bäckhed F, Ding H, Wang T, Hooper LV, Gou YK, Nagy A (2004) The gut microbiota as an environmental factor that regulates fat storage. PNAS USA 101:15718–15723

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  3. Butt RL, Volkoff H (2019) Gut microbiota and energy homeostasis in fish. Front Endocrinol 10:9

    Article  Google Scholar 

  4. Cardona E, Gueguen Y, Magre 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  5. Chaiyapechara S, Rungrassamee W, Suriyachay I, Kuncharin Y, Klanchui A, Karoonuthaisiri N, Jiravanichpaisal P (2012) Bacterial community associated with the intestinal tract of P. monodon in commercial farms. Microb Ecol 63:938–953

    PubMed  Article  Google Scholar 

  6. Chen WY, Ng TH, Wu JH, Chen JW, Wang HC (2017) Microbiome dynamics in a shrimp grow-out pond with possible outbreak of Acute Hepatopancreatic Necrosis Disease. Sci Rep 7:9395

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  7. CIBA Annual report 2016–2017 (2017) Central Institute of Brackishwater Aquaculture, Chennai, Tamil Nadu, India p 36–40

  8. Cornejo-Granados F, Lopezzavala AA, Gallardobecerra L, Mendozavargas A, Sanchez F, Vichido R et al (2017) Microbiome of Pacific whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Sci Rep 7:11783

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  9. Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J (2017) MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nuc Acid Res 45:181–188

    Article  CAS  Google Scholar 

  10. Fan L, Li QX (2019) Characteristics of intestinal microbiota in the Pacific white shrimp Litopenaeus vannamei differing growth performances in the marine cultured environment. Aquaculture 505:450–461

    Article  Google Scholar 

  11. Fan LF, Wang ZL, Chen MS, Qu YX, Li JY, Zhou AG, Xie SL, Zeng F, Zou JX (2019) Microbiota comparison of Pacific white shrimp intestine and sediment at freshwater and marine cultured environment. Sci Tot Environ 657:1194 1204

    Google Scholar 

  12. Fraune S, Zimmer M (2008) Host-specificity of environmentally transmitted mycoplasma-like isopod symbionts. Environ Microbiol 10(10):2497–2504

    CAS  PubMed  Article  Google Scholar 

  13. Frisch K, Småge SB, Johansen R, Duesund H, Brevik OJ, Nylund A (2018) Pathology of experimentally induced mouth rot caused by Tenacibaculum maritimum in Atlantic salmon smolts. PLoS One 13(11):e0206951

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    CAS  Article  Google Scholar 

  15. Garibay-Valdez E, Martínez-Córdova LR, Vargas-Albores F, Gollas-Galván T, Lago-Leston A, Calderón K, Martínez-Porchas M (2018) Biofilm consumption shapes the intestinal microbiota of shrimp (Penaeus vannamei). Aquacult Nutr 25(2):427–435

    Article  CAS  Google Scholar 

  16. 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 Bioinfo 16:169

    Article  Google Scholar 

  17. Hooper LV (2004) Bacterial contributions to mammalian gut development. Trends Microbiol 12:129–134

    CAS  PubMed  Article  Google Scholar 

  18. Kho ZY, Lal SK (2018) The human gut microbiome-a potential controller of wellness and diseases. Front Microbiol 9:1835

    PubMed  PubMed Central  Article  Google Scholar 

  19. Li E, Xu C, Wang X, Wang S, Zhao Q, Zhang Z, Qin GJ, Chen L (2018) Gut microbiota and its modulation for healthy farming of Pacific White Shrimp Litopenaeus vannamei. Rev Fish Sci Aquacult 26:381–399

    Article  Google Scholar 

  20. Li Y, Hu X, Yang S, Zhou J, Zhang T, Qi L, Sun X, Fan M, Xu S, Cha M, Zhang M, Lin S, Liu S, Hu D (2017) Comparative analysis of the gut microbiota composition between captive and wild forest musk deer. Front Microbiol 8:1705

    PubMed  PubMed Central  Article  Google Scholar 

  21. Liu F, Liu G, Li F (2016) Characterization of two pathogenic Photobacterium strains isolated from Exopalaemon carinicauda causing mortality of shrimp. Aquaculture 464:129–135

    Article  Google Scholar 

  22. Liu H, Wang L, Liu M, Wang B, Jiang K, Ma S, Li Q (2011) The intestinal microbial diversity in Chinese shrimp (Fenneropenaeus chinensis) as determined by PCR–DGGE and clone library analyses. Aquaculture 317:32–36

    CAS  Article  Google Scholar 

  23. Ma X, Sun B, Zhu F (2018) Molecular cloning of Kuruma shrimp Marsupenaeus japonicus endonuclease-reverse transcriptase and its positive role in white spot syndrome virus and Vibrio alginolyticus infection. Fish Shellfish Immunol 73:297–308

    CAS  PubMed  Article  Google Scholar 

  24. Md-Zoqratt MZH, 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  25. Metian M, Troell M, Christensen V, Steenbeek J, Pouil S (2020) Mapping diversity of species in global aquaculture. Rev Aquacult 12:1090–1100

    Article  Google Scholar 

  26. Nayak S (2010) Probiotics and immunity: A fish perspective. Fish Shellfish Immunol 29(1):2–14

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. Nelson TM, Rogers TL, Brown MV (2013) The gut bacterial community of mammals from marine and terrestrial habitats. PLoS One 8(12):e83655

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  28. Oxley AP, Shipton W, Owens L, McKay D (2002) Bacterial flora from the gut of the wild and cultured banana prawn, Penaeus merguiensis. J Appl Microbiol 93(2):214–223

    CAS  PubMed  Article  Google Scholar 

  29. Pérez-Pascual D, Lunazzi A, Magdelenat G, Rouy Z, Roulet A, Lopez-Roques C, Larocque R, Barbeyron T, Gobet A, Michel G, Bernardet JF, Duchaud E (2017) The complete genome sequence of the fish pathogen Tenacibaculum maritimum provides insights into virulence mechanisms. Front Microbiol 8:1542

    PubMed  PubMed Central  Article  Google Scholar 

  30. Qi C, Wang L, Jiang K, Wang M, Zhao W, Wang B (2017) Transcriptomic and morphological analyses of Litopenaeus vannamei intestinal barrier in response to Vibrio paraheamolyticus infection reveals immune response signatures and structural disruption. Fish Shellfish Immunol 70:437–450

    CAS  PubMed  Article  Google Scholar 

  31. Qiao F, Liu Y, Sun Y, Wang X, Chen K, Li T, Li E, Zhang M (2017) Influence of different dietary carbohydrate sources on the growth and intestinal microbiota of Litopenaeus vannamei at low salinity. Aquacult Nutr 23:444–452

    CAS  Article  Google Scholar 

  32. Ramírez 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 

  33. Ramírez C, Romero J (2017a) The microbiome of Seriola lalandi of wild and aquaculture origin reveals differences in composition and potential function. Front Microbiol 8:1844

    PubMed  PubMed Central  Article  Google Scholar 

  34. Remany M, Cyriac D, Nagaraj S, Rao B, Panda A, Kumar J, Samraj Y (2010) Specific pathogen-free assurance of imported Pacific white shrimp Litopenaeus vannamei (Boone, 1931 in the Aquatic Quarantine Facility, Chennai. Curr Sci 99(12):1656–1658

    Google Scholar 

  35. Ringø E, Zhou Z, Vecino JLG, Wadsworth S, Roomero J, Krogdahl Å, Olsen RE, Dimitroglou A, Foey A, Davies S, Owen M, Lauzon HL, Martinsen LL, De Schryver P, Bossier P, Sperstad S, Merrifield DL (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquacult. Nutr 22:219–282

    Google Scholar 

  36. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5(10):1595–1608

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Rungrassamee W, Klanchui A, Chaiyapechara S, Maibunkaew S, Tangphatsornruang S (2013) Bacterial population in intestines of the Black Tiger Shrimp (Penaeus monodon) under different growth stages. PLoS One 8(4):e60802

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  39. 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 Invert Pathol 133:12–19

    CAS  Article  Google Scholar 

  40. Sajeela KA, Gopalakrishnan A, Basheer VS, Mandal A, Bineesh KK, Grinson G, Gopakumar SD (2019) New insights from nuclear and mitochondrial markers on the genetic diversity and structure of the Indian white shrimp Fenneropenaeus indicus among the marginal seas in the Indian Ocean. Mol Phylogenet Evol 136:53–64

    CAS  PubMed  Article  Google Scholar 

  41. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB (2009) Introducing Mothur: open-source. platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Småge SB, Frisch K, Brevikm OJ, Watanabe K, Nylund A (2016) First isolation, identification and characterization of Tenacibaculum maritimum in Norway, isolated from diseased farmed sea lice cleaner fish Cyclopterus lumpus L. Aquaculture 464:178–184

    Article  Google Scholar 

  43. Suo Y, Li E, Li T, Jia Y, Qin JG, Gu Z, Chen L (2017) Response of gut health and microbiota to sulfide exposure in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 63:87–96

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  45. Thompson J, Gregory S, Plummer S, Shields RJ, Rowley AF (2010) An in vitro and in vivo assessment of the potential of Vibrio spp. as probiotics for the Pacific White shrimp, Litopenaeus vannamei. J Appl Microbiol 109:1177–1187

    CAS  PubMed  Article  Google Scholar 

  46. Urbanczyk H, Ast JC, Dunlap PV (2011) Phylogeny, genomics, and symbiosis of Photobacterium. FEMS Microbiol Rev 35:324–342

    CAS  PubMed  Article  Google Scholar 

  47. Vandenberghe J, Verdonck L, Robles-Arozarena R, Rivera G, Bolland A, Balladares M, Gomez-Gil B, Calderon J, Sorgeloos P, Swings J (1999) Vibrios associated with Litopenaeus vannamei larvae, postlarvae, broodstock, and hatchery probionts. Appl Environ Microbiol 65:2592–2597

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. Vaseeharan B, Sundararaj S, Murugan T, Chen J (2007) Photobacterium damselae ssp. damselae associated with diseased black tiger shrimp Penaeus monodon (Fabricius) in India. Let Appl Microbiol 45:82–86

    CAS  Article  Google Scholar 

  49. Velázquez-Lizárraga AE, Juárez-Morales JL, Racotta IS, Villarreal-Colmenares H, Valdes-Lopez O, Luna-González A, Rodríguez-Jaramillo C, Estrada N, Ascencio F (2019) Transcriptomic analysis of Pacific white shrimp (Litopenaeus vannamei, Boone 1931) in response to acute hepatopancreatic necrosis disease caused by Vibrio parahaemolyticus. PLoS ONE 14:e0220993

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  50. Wang CZ, Lin GR, Yan T, Zheng ZP, Chen B, Sun FL (2014) The cellular community in the intestine of the shrimp Penaeus penicillatus and its culture environments. Fish Sci 80:1001–1007

    CAS  Article  Google Scholar 

  51. Wang J, Uang 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 Immunol 84:130–137

    PubMed  Article  Google Scholar 

  52. 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(16):5261–5267

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Wei H, Wang H, Tang L, Wang C (2019) High-throughput sequencing reveals the core gut microbiota of the mud crab (Scylla paramamosain) in different coastal regions of southern China. BMC Genom 20:829

    Article  CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. Yan Q, Li J, Yu Y, Wang J, He Z, Van NJD, Zhou J (2016) Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ Microbiol 18:4739–4754

    CAS  PubMed  Article  Google Scholar 

  56. Zeng S, Huang Z, Hou D, Liu J, Weng S, He J (2017) Composition, diversity and function of intestinal microbiota in pacific white shrimp (Litopenaeus vannamei) at different culture stages. PeerJ 5:e3986

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  57. Zeng S, Khoruamkid S, Kongpakdee W, Wei D, Yu L, Wang H, Deng Z, Weng S, Huang Z, He J, Satapornvanit K (2020) Dissimilarity of microbial diversity of pond water, shrimp intestine and sediment in Aquamimicry system. AMB Express 10:180

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Zheng, Y., Yu, M., Liu, Y., Su, Y., Xu, T., Yu. M., Zhang, X. H., 2017. Comparison of cultivable bacterial communities associated with Pacific white shrimp (Litopenaeus vannamei) larvae at different health statuses and growth stages. Aquaculture 451, 163-169.

  59. Zhang M, Sun Y, Liu Y, Qiao F, Chen L, Liu W, Du Z, Li E (2016) Response of gut microbiota to salinity change in two euryhaline aquatic animals with reverse salinity preference. Aquaculture 454:72–80

    CAS  Article  Google Scholar 

  60. 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

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Acknowledgements

We acknowledge Director, ICAR-CIBA for providing research infrastructures to carry-out the study.

Funding

This work was supported by Consortia Research Platform (CRP) on Vaccine and Diagnostics (CRP-V&D) 1007611.

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Contributions

Prasanna Kumar Patil and Vinay Tharabenahalli Nagaraju conceived and designed the project. Vinay Tharabenahalli Nagaraju collected the samples. Satheesha Avunje and Viswanathan Baskaran extracted the DNA and sequencing. Sudeep Darbhe Ghate and Vinay Tharabenahalli Nagaraju conducted bioinformatic analysis. Prasanna Kumar Patil, Vinay Tharabenahalli Nagaraju and Sudeep Darbhe Ghate analyzed the data, and wrote the manuscript. All authors reviewed and approved the manuscript.

Corresponding author

Correspondence to Tharabenahalli Nagaraju Vinay.

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Authors declare no conflict of interest.

Ethics approval

The research undertaken complies with the current animal welfare laws in India. The experimental animal Penaeus indicus is not an endangered shrimp; the provisions of the Govt. of India’s Wildlife Protection Act of 1972 are not applicable for experiments on this shrimp.

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Patil, P.K., Vinay, T.N., Ghate, S.D. et al. 16 S rRNA gene diversity and gut microbial composition of the Indian white shrimp (Penaeus indicus). Antonie van Leeuwenhoek (2021). https://doi.org/10.1007/s10482-021-01658-9

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Keywords

  • Aquaculture
  • Indian white shrimp (Penaeus indicus)
  • Gut microbiota
  • MOTHUR