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Symbiosis

, Volume 76, Issue 1, pp 51–62 | Cite as

Metatrancriptomic analysis from the Hepatopancreas of adult white leg shrimp (Litopenaeus vannamei)

  • Raul Enrique Valle-Gough
  • Javier Eduardo Apodaca-Hernández
  • Mauricio Rodriguez-Dorantes
  • María Leticia Arena-Ortiz
Article
  • 153 Downloads

Abstract

White leg shrimp (Litopenaeus vannamei) is a widely cultured shellfish in coastal areas of the Pacific and is considered one of the dominant crustaceans in aquaculture, globally. There is currently no information regarding the functional role of the microbiome of L. vannamei. In this study Next Generation Sequencing techniques were used to generate the metatranscriptome of the hepatopancreas from adult individuals of this species. The functional role of the microbiome showed that the most represented bacterial phylum consisted of Proteobacteria, Firmicutes and Actinobacteria, in which several bacterial classes produce different sets of hydrolytic enzymes. The most represented functions in the microbiome were related to the metabolism of proteins, amino acids, carbohydrates and lipids. These systems were also highly represented in L. vannamei. This response suggests that the nutrient absorption involves the joint participation of the host and the microbiome. A similar behavior was observed in abiotic stress related genes in L. vannamei and the microbial communities. There was a high representation in both systems, suggesting that the host-microbiome has adapted to the environmental fluctuations. Pathogens were found in this study in low titers, which are common in marine organisms; and several mechanisms that participate in the pathogenic response of L. vannamei were identified such as: proteolytic enzymes and cell communication mechanisms. Over a thousand genic microbial products were identified in the metatranscriptome of L. vannamei including the presence of several genes related to metabolic functions, stress and antibiotic resistance. This study provides evidence of the microbiome interactions in L. vannamei during the culture of this species and the different factors that could affect the microbial composition and gene expression.

Keywords

Microbiome Metatranscriptomics NGS Functional analysis 

Notes

Acknowledgements

To the National Council of Science and Technology (CONACyT) for the funding of this project and the General Direction of Academic Personal Affairs (DGAPA) for the postdoctoral grant for REVG. To AquaPacific (Mazatlan, Sinaloa, Mexico) especially to: Bruno Gomez-Gil, Sonia Soto and Daniel Palacios for provide the biological material collection.

References

  1. Aprill A (2017) Marine animal microbiomes: toward understanding host-microbiome interaction in a changing ocean. Frontiers in marine. Science 4:222.  https://doi.org/10.3389/frmars.2017.00222 Google Scholar
  2. Bizans JE, Macklaim JM, Gloor GM, Reid G (2014) Bacterial metatranscriptome analysis of a probiotic yogurt using a RNA-Seq approach. Int Dairy J 39:284–292CrossRefGoogle Scholar
  3. Booijink CCGM, Boekhorst J, Zoetendal EG, Smidt H, Kleerebezem M, de Vos M (2010) Metatranscriptome analysis of the human fecal microbiota reveals subject-specific expression profiles, with genes encoding proteins involved in carbohydrate metabolism being dominantly expressed. Appl Environ Microbiol 76(16):5533–5540.  https://doi.org/10.1128/AEM.00502-10 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cao XH, Schmutzer T, Scholz U, Pecinka A, Schubert I, GTH V (2015) Metatranscriptomic analysis reveals host-microbiome interactions in traps of carnivorous Genlisea species. Front Microbiol 6:526.  https://doi.org/10.3389/fmxcb.2015.00526. PubMedPubMedCentralGoogle Scholar
  5. Chan KG, Ismail Z (2015) Tropical soil metagenome library reveals complex microbial assemblage. BioRxiv:1–25.  https://doi.org/10.1101/018895
  6. Chavez-Calvillo G, Pérez-Rueda E, Lizama G, Zúñiga JJ, Gaxiola G, Cuzon G, Arena-Ortíz L (2010) Differential gene expression in Litopenaeus vannamei shrimp in response to diet changes. Aquaculture 300(1–4):137–141.  https://doi.org/10.1016/j.aquaculture.2009.11.027 CrossRefGoogle Scholar
  7. Chen X, Zeng D, Chen X, Xie D, Zhao Y, Yang C, Li Y, Ma N, Li M, Yang Q, Liao Z, Wang H (2013) Transcriptome analysis of Litopenaeus vannamei in response to white spot Sindrome virus infection. PLoS One 8(6):e73218.  https://doi.org/10.1371/journal.pone.0073218 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chiu C, Guu YK, Liu CH, Pang TZ, Chen W (2007) Immune responses and gene expression in white shrimp, Litopenaeus vannamei, induced by Lactobacillus plantarum. Fish and shellfish. Immunology 23(2):364–377Google Scholar
  9. Chomzcsinsky P, Sacchi N (1987) Single-step method for RNA isolation by acid guanidinium thyocyanate-phenol-chloroform extraction. Ann Biochem 162(1):156–159.  https://doi.org/10.1006/abio.1987.9999 CrossRefGoogle Scholar
  10. Collado L, Figueroa MJ (2011) Taxonomy, epidemiology and clinical reference of the genus Arcobacter. Clin Microbiol Rev 24(1):174–192.  https://doi.org/10.1128/CMR.00034-10 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Costa PC, Rei MP, Ávila MP, Leite LR, De Araujo FMG, Salim ACM, Oliveira G, Barbosa F, Chartone-Souza E, Nascmiento AMA (2015) Metagenome of a microbial community Inhabitating a metal-rich tropical stream sediment. PLoS One 10(3):e0119465.  https://doi.org/10.1371/journal.pone.0119465 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next generation sequencing. Nat Rev Genet 12(7):499–510.  https://doi.org/10.1038/nrg3012 CrossRefPubMedGoogle Scholar
  13. Degli-Esposti M, Martinez-Romero E (2017) The functional microbiome of arthropods. PLoS One 12(5):e0176573.  https://doi.org/10.1371/journal.pone.0176573 CrossRefPubMedPubMedCentralGoogle Scholar
  14. DePristo MA, Banks E, Poplin RE, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M, McKenna A, Fennell TJ, Kernystsky AM, Sivachenko AY, Cibulskis K, Gabriel SB, Altshuller D, Daly MJ (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491–498.  https://doi.org/10.1038/ng.806 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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.  https://doi.org/10.1111/jfd.12624 CrossRefPubMedGoogle Scholar
  16. Donachie SP, Saborowski R, Peters G, Buchholz F (1995) Bacterial digestive enzyme activity in the stomach and hepatopancreas of Meganycitiphanes norvergica (M. Sars, 1857). J Exp Mar Biol Ecol 188(2):151–165.  https://doi.org/10.1016/0022-0981(94)00193-H CrossRefGoogle Scholar
  17. Ekblom R, Galindo J (2011) Application of next generation sequencing in molecular ecology of non-model organisms. Heredity 107(1):1–15.  https://doi.org/10.1038/hdy.2010.152 CrossRefPubMedGoogle Scholar
  18. Elshire RJ, Glaubitz JC, Sun Q, Pland JA, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for diversity species. PLoS One 6(5):e19379.1CrossRefGoogle Scholar
  19. Food and Agriculture Organization of the United Nations (FAO) (2015) Global Aquaculture Production, 1950–2015 http://wwwfaoorg/fishery/statistics/global-aquaculture-production/query/es Accesed 15 April 2017
  20. Gamboa-Delgado J, Molina-Poveda C, Cahu C, (2003) Digestive enzyme activity and food ingesta in juvenile shrimp Litopenaeus vannamei (Boone, 1931) as a function of body weight. Aquaculture Research 34 (15):1403–1411Google Scholar
  21. Ghaffari N, Sanchez-Flores A, Doon R, García-Orozco KD, Chen PL, Ochoa-Leyva A, López-Zavala A, Carrasco S, Hong C, Brieba LG, Rudiño-Piñera E, Blood PD, Sawyer JD, Johnson CD, Dindo SV, Sotelo-Mundo RR, Critiscello MF (2014) Novel transcriptome assembly and improved annotation of the white leg shrimp (Litopenaeus vannamei), a dominant crustacean in global seafood mariculture. Sci Rep 4(7081):1–10Google Scholar
  22. Gilford SM, Sharma S, Rinta-Kanto JM, Moran MA (2011) Quantitative analysis of a deeply sequence marine microbial metatranscriptome. ISME J 5(3):461–472.  https://doi.org/10.1038/ismej.2010.141 CrossRefGoogle Scholar
  23. Gillespie DE, Brady SF, Betterman AD, Cianciotto NP, Liles MR, Rondon MR, Clardy J, Goodman RM, Handelsman J (2002) Isolation of antibiotics Turbomycin a and B from a metagenomic library of soil microbial DNA. Appl Environ Microbiol 68(9):4301–4306.  https://doi.org/10.1128/AEM.68.9.4301-4306.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Godinez-Siordia DE, Chavez-Sanchez MC, Gomez-Jiménez S (2011) Epicontinental aquaculture of the Paciffic white shrimp, Litopenaeus vannamei, (Boone, 1931). Tropical and Subtropical Agroecosystems 14:55–62Google Scholar
  25. Gomez-Gil B, Tron-Mayén L, Roque A, Turnbull JF, Inglis V, Guerra-Flores A (1998) Species of Vibrio isolated from the hepatopancreas, haemolymph and digestive tract of a population of healthy juvenile Penaeus vannamei. Aquaculture 163(1-2):1–9.  https://doi.org/10.1016/S0044-8486(98)00162-8 CrossRefGoogle Scholar
  26. Gullian M, Thompson F, Rodriguez J (2004) Selection of probiotic bacteria and study of their immunostimulatory effect in Penaeus vannamei. Aquaculture 233(1-4):1–14.  https://doi.org/10.1016/j.aquaculture.2003.09.013 CrossRefGoogle Scholar
  27. Hu KH, Leung PC (2007) Food digestion by cathepsin L and digestion-related rapid cell differentiation in shrimp hepatopancreas. Comp Biochem Physiol B 146(1):69–80.  https://doi.org/10.1016/j.cbpb.2006.09.010 CrossRefPubMedGoogle Scholar
  28. 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. 47:1737–1746Google Scholar
  29. Ji PF, Yao CL, Wan ZY (2009) Immune response and gene expression in shrimp (Litopenaeus vannamei) hemocytes and hepatopancreas against some pathogen-associated molecular patterns. Fish and shellfish. Immunology 27:563–570Google Scholar
  30. Juzeniene A, Tam TTT, Iani V, Moan J (2013) The action spectrum of photodegradation in aqueous solutions. J Photochem Photobiol B Biol 126(5):11–16.  https://doi.org/10.1016/j.jphotobiol.2013.05.011 CrossRefGoogle Scholar
  31. Kanokatrana P, Uengwetwanit RU, Bunterngsook B, Nimchua T, Tangphatsornruang S, Plengvidhya V, Champreda V, Eurwilaichitr L (2011) Insights into the phylogeny and metabolic potential of a primary tropical peat swamp Forest microbial community by metagenomic analysis. Microb Ecol 61(3):518–528.  https://doi.org/10.1007/s00248-010-9766-7 CrossRefGoogle Scholar
  32. Leimenena MM, Ramiro-Garcia J, Davids M, Van den Bogert B, Smidt H, Smid JE, Boekhorst J, Zotendal EG, Schaap PJ, Kleerebezem M (2013) A comprehensive metatranscriptome analysis pipeline and its validation using small intestine microbiota datasets. BMC Genomics 14(1):530–543.  https://doi.org/10.1186/1471-2164-14-530 CrossRefGoogle Scholar
  33. Li C, Wang S, Chen Y, Yu X, Lü L, Zhang H, Xu X (2012) Analysis of Litopenaeus vannamei transcriptome using the next-generation DNA sequencing Technoque. PLoS One 7(10):e47442.  https://doi.org/10.1371/journal.pone.0047442 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lowe RGT, Cassin A, Grandaubert J, Clark BL, Van de Wouw AP, Rouxel T, Howlett BH (2014) Genomes and transcriptomes of Partners in Plant-Fungal- Interactions between canola (Brassica napus) and two Leptosphaeria species. PLoS One 9(7):e103098.  https://doi.org/10.1371/journal.pone.0103098 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Luis-Villaseñor IE, Castellanos-Cervantes T, Gomez-Gil B, Carrillo-García AE, Campa-Córdova AI, Ascencio F (2013) Probiotics in the intestinal tract of juvenile whiteleg shrimp Litopenaeus vannamei: modulation of the bacterial community. World journal of Microbiolog and. Biotechnology 29:257–265Google Scholar
  36. Pathak SC, Ghosh SK, Palanisamy K (2000) The use of chemicals in aquaculture in India. In: Arthur JR, Lavilla-Pitogo CR, Subasinghe RP (eds) Use of Chemicals in Aquaculture in Asia. Proceedings of the meeting on the use of Chemicals in Aquaculture in Asia 20–22 may 1996, Tigbauan, Iloilo, Philippines. Aquaculture Department, Southeast Asian Fisheries Development Center, pp 87–112Google Scholar
  37. Rappold H, Bacher A (1974) Bacterial degradation of folic acid. J Gen Microbiol 85(2):283–290.  https://doi.org/10.1099/00221287-85-2-283 CrossRefPubMedGoogle Scholar
  38. Reisenfeld CS, Goodman RM, Handelsman J (2004) Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ Microbiol 6(9):981–989.  https://doi.org/10.1111/j.1462-2920.2004.00664.x CrossRefGoogle Scholar
  39. Robalino J, Almeida JS, McKillen D, Colglazier J, Trent HF III, Chen YA, Peck ME, Browdy CL, Chapman RW, Warr GW, Gross PS (2007) Insights into the immune transcriptome of the shrimp Litopenaeus vannamei: tissue-specific expression profiles and transcriptomic responses to immune challenge. Physiol Genomics 29(1):44–56.  https://doi.org/10.1152/physiolgenomics.00165.2006 CrossRefPubMedGoogle Scholar
  40. Rungrassamee W, Klanchul A, Maibunkaew A, Chalyapechara 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.  https://doi.org/10.1371/journal.pone.0091853 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Silva AJ, Benitez JA (2016) Vibrio cholerae biofilms and cholera pathogenesis. PLoS Negl Trop Dis 10(2):e0004330.  https://doi.org/10.1371/journal.pntd.0004330 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Soleimani N, Hoseinifar SH, Merrifield DL, Barati M, Abadi ZH (2012) Dietary supplementation of fructooligosaccharide (FOS) improves the innate immune response, stress resistance, digestive enzyme activity and growth performance of Caspian roach (Rutilus rutilus) fry. Fish and shellfish. Immunology 32:316–321Google Scholar
  43. Su JQ, Wei B, CY X, Qiao M, Zhu GY (2014) Functional metagenomic characterization of antibiotic resistance genes in agricultural soils from China. Environ Int 65:9–15.  https://doi.org/10.1016/j.envint.2013.12.010
  44. Tassanakajon A, Klinbunga S, Paunglarp N, Rimphanitchayakit V, Udomkit A, Jitrapakdee S, Sritunyalucksana K, Phongdara A, Pongsomboon S, Supungul P, Tang S, Kuphanumart K, Pichyangkura R, Lursinsap C (2006) Penaeus monodon gene discovery project: the generation of an EST collection and establishment of a database. Gene 384:104–112.  https://doi.org/10.1016/j.gene.2006.07.012 CrossRefPubMedGoogle Scholar
  45. Teo J, Liew Y, Lee W, Lay-Hoon KA (2014) Prolonged infusion versus intermittent boluses of β-lactam antibiotics for treatment of acute infections: a meta-analysis. Int J Antimicrob Agents 43(5):403–411.  https://doi.org/10.1016/j.ijantimicag.2014.01.027 CrossRefPubMedGoogle Scholar
  46. Tsai WT (2010) Current status and regulatory aspects of pesticides considered to be persistent organic pollutants (POPs) in Taiwan. Int J Environ Res Public Health 7(10):3615–3627.  https://doi.org/10.3390/ijerph7103615 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tsang WS, Quackenbush LS, Chow BKC, Tiu SHK, He JG, Chan SM (2003) Organization fo the vitellogenin gene: evidence of multple genes and tissue specific expression by the ovary and hepatopancreas. Gene 303:99–109.  https://doi.org/10.1016/S0378-1119(02)01139-3
  48. Tuyub-Tzuc J, Rendiz-Escalante D, Rojas-Herrera R, Gaxiola-Cortés G, Arena-Ortiz L (2014) Microbiota from Litopenaeus vannamei: digestive tract microbial community of Pacific white shrimp (Litopenaeus vannamei). SpringerPlus 3(1):280.  https://doi.org/10.1186/2193-1801-3-280 CrossRefGoogle Scholar
  49. Utiswannakul P, Sangchai S, Rengpipat S (2011) Enhanced growth of black tiger shrimp Penaeus monodon by dietary supplementation with Bacillus (BP11) as a probiotic. J Aquat Res Dev S1:006Google Scholar
  50. Wei J, Zhang X, Yu Y, Huang H, Li F, Xiang J (2014) Comparative transcriptomic characterization of the early development in Pacific white shrimp Litopenaeus vannamei. PlosOne 9(9):e106201.  https://doi.org/10.1371/journal.pone.0106201 CrossRefGoogle Scholar
  51. Xie L, Zhang L, Zhong Y, Liu N, Long Y, Wang S, Zhou X, Zhou Z, Huang Y, Wang Q (2012) Profiling the metatranscriptome of the protistan community in Coptotermes formosanus with emphasis on the lignocellulolytic system. Genomics 99(4):246–255.  https://doi.org/10.1016/j.ygeno.2012.01.009 CrossRefPubMedGoogle Scholar
  52. Xiong X, Frank DN, Robertson CE, Hung SS, Markle J, Canty AJ, McCoy KD, Macpherson AJ, Poussier P, Danska JS, Parkinson J (2012) Generation and analysis of mouse intestinal Metatranscriptome through Illumina based RNA-sequencing. PLoS One 7(4):e36009.  https://doi.org/10.1371/journal.pone.0036009 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Yun J, Kang S, Park S, Yoon H, Kim MJ, Heu S, Ryu S (2004) Characterization of a novel Amylolytic enzyme by a gene from a soil-derived metagenomic library. Appl Environ Microbiol 70(12):7229–7235.  https://doi.org/10.1128/AEM.70.12.7229-7235.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Zeng D, Chen X, Xie D, Zhao Y, Yang C, Li Y, Ma N, Peng M, Yang Q, Liao Z, Wang H, Chen X (2013) Transcriptome analysis of Pacific white shrimp (Litopenaeus vannmei) Hepatopancreas in response to Taura Sindrome virus (TSV) experimental infection. PLoS One 8(2):e57515.  https://doi.org/10.1371/journal.pone.0057515 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zimmer M, Danko JP, Pennings SC, Danford AR, Ziegler A, Uglow RF, Carefoot TH (2001) Hepatopancreatic endosymbionts in coastal isopods (Crustacea: Isopoda), and their contribution to digestion. Mar Biol 138(5):955–963.  https://doi.org/10.1007/s002270000519 CrossRefGoogle Scholar
  56. Zokaeifar H, Balcázar JL, Saad C, Kamarudin MS, Sijam K, Arshad A, Nejat N (2012) Effects of Bacillus subtilis on the growth performance, digestive enzymes, immune gene expression and disease resistance of white shrimp, Litopenaeus vannamei. Fish and shellfish. Immunology 33:683–689Google Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Raul Enrique Valle-Gough
    • 1
  • Javier Eduardo Apodaca-Hernández
    • 2
  • Mauricio Rodriguez-Dorantes
    • 3
  • María Leticia Arena-Ortiz
    • 1
  1. 1.Unidad de Ciencias y Tecnología de la UNAM, YucatánSisalMexico
  2. 2.Bibliotecas Genómicas S.A, de C.VMéridaMexico
  3. 3.Instituto Nacional de Medicina GenómicaCiudad de MéxicoMexico

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