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Rapid Change of Microbiota Diversity in the Gut but Not the Hepatopancreas During Gonadal Development of the New Shrimp Model Neocaridina denticulata

Marine Biotechnology volume 17, pages 811–819 (2015)Cite this article

Abstract

During evolution of animals, their co-evolution with bacteria has generally been ignored. Recent studies have provided evidences that the symbiotic bacteria in the animal gut can either be essential or contributing to the plasticity of the host. The Crustacea includes crab, crayfish, lobster, and shrimp and represents the second largest subphylum on the planet. Although there are already studies investigating the intestinal bacterial communities in crustaceans, none of them has examined the microbiota in different parts of the digestive system during the gonad development of the host. Here, we utilized a new shrimp model Neocaridina denticulata and sequenced the 16S rRNA using the Ion Torrent platform to survey the bacterial populations colonizing the hepatopancreas, foregut, and intestine, including midgut and hindgut, of the early, mid, and late ovarian maturation stages of the shrimp. The predominant bacteria phylum was found to be Proteobacteria, with more than 80 % reads from the gut flora at the early gonad development belonged to a Coxiella-type bacterium. Distinct bacterial communities can be detected between the hepatopancreas and gut, although no significant difference could be revealed between the different regions of the gut investigated. Surprisingly, during the gonad development, bacterial diversity changed rapidly in the gut but not the hepatopancreas. This study provides the first evidence that microbiota modified differentially in specific regions of the digestive tract during gonadal development of crustaceans.

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References

  • Adachi K, Toriyama K, Azekura T, Morioka K, Tongnunui P, Ikejima K (2012) Potent cellulase activity in the hepatopancreas of mangrove crabs. Fish Sci 78:1309–1314

    CAS  Article  Google Scholar 

  • Andreotti R, Pérez de León AA, Dowd SE, Guerrero FD, Bendele KG, Scoles GA (2011) Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol 11:6

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Andriantahina F, Liu X, Feng T, Xiang J (2013) Current status of genetics and genomics of reared penaeid shrimp: information relevant to access and benefit sharing. Mar Biotechnol (NY) 15(4):399–412

    Article  Google Scholar 

  • Appleby JC (1955) The isolation and classification of proteolytic bacteria from the rumen of the sheep. J Gen Microbiol 12:526–533

    CAS  Article  PubMed  Google Scholar 

  • Bouskra D, Brézillon C, Bérard M, Werts C, Varona R, Boneca IG, Eberl G (2008) Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456:507–510

    CAS  Article  PubMed  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Ceccaldi HJ (1989) Anatomy and physiology of digestive tract of crustacean decapods reared in aquaculture. Adv Trop Aquacult 9:243–259

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Chu KH (1999) Morphometric analysis and reproductive biology of the crab Charybdis affinis (Decapoda, Brachyura, Portunidae) from the Zhujiang Estuary, China. Crustaceana 72:647–658

    Article  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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Diaz Heijtz R, Wang S, Anuar F, Qian Y, Björkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 108:3047–3052

    Article  PubMed  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    CAS  Article  PubMed  Google Scholar 

  • Felgenhauer BE (1992) Internal anatomy of the Decapoda. In: Harrison R and Humes A (eds) Microscopic anatomy of the invertebrates, vol 10. Wiley-Liss Press, New York, p 45–75

  • Freese HM, Schink B (2011) Composition and stability of the microbial community inside the digestive tract of the aquatic crustacean Daphnia magna. Microb Ecol 62:882–894

    Article  PubMed  Google Scholar 

  • French SS, Moore MC (2008) Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus. Gen Comp Endocrinol 155:148–156

    CAS  Article  PubMed  Google Scholar 

  • Givens CE, Burnett KG, Burnett LE, Hollibaugh JT (2013) Microbial communities of the carapace, gut, and hemolymph of the Atlantic blue crab, Callinectes sapidus. Mar Biol 160:2841–2851

    Article  Google Scholar 

  • Harris JM (1993) The presence, nature, and role of gut microflora in aquatic invertebrates: a synthesis. Microb Ecol 25:195–231

    CAS  Article  PubMed  Google Scholar 

  • Homonnay ZG, Kéki Z, Márialigeti K, Tóth EM (2012) Bacterial communities in the gut of the freshwater copepod Eudiaptomus gracilis. J Basic Microbiol 52:86–90

    Article  PubMed  Google Scholar 

  • Huang Z, Li X, Wang L, Shao Z (2015) Changes in the intestinal bacterial community during the growth of white shrimp, Litopenaeus vannamei. Aquac Res. doi:10.1111/are.12628

    Google Scholar 

  • Jiang H, Li F, Zhang J, Zhang J, Huang B, Yu Y, Xiang J (2014) Comparison of protein expression profiles of the hepatopancreas in Fenneropenaeus chinensis challenged with heat-inactivated Vibrio anguillarum and white spot syndrome virus. Mar Biotechnol (NY) 16(1):111–123

    CAS  Article  Google Scholar 

  • Kenny NJ, Sin YW, Shen X, Zhe Q, Wang W, Chan TF, Tobe SS, Shimeld SM, Chu KH, Hui JH (2014) Genomic sequence and experimental tractability of a new decapod shrimp model, Neocaridina denticulata. Mar Drugs 12:1419–1437

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Kung SY, Chan SM, Hui JH, Tsang WS, Mak A, He JG (2004) Vitellogenesis in the sand shrimp, Metapenaeus ensis: the contribution from the hepatopancreas-specific vitellogenin gene (MeVg2). Biol Reprod 71:863–870

    CAS  Article  PubMed  Google Scholar 

  • Leaño EM, Lavilla-Pitogo CR, Paner MG (1998) Bacterial flora in the hepatopancreas of pond-reared Penaeus monodon juveniles with luminous vibriosis. Aquaculture 164:367–374

    Article  Google Scholar 

  • Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848

    CAS  Article  PubMed  Google Scholar 

  • 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 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Mackie RI, Wilkins CA (1988) Enumeration of anaerobic bacterial microflora of the equine gastrointestinal tract. Appl Environ Microbiol 54:2155–2160

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maeda M, Shibata A, Biswas G, Horenaga H, Kono T, Itami T, Sakai M (2014) Isolation of lactic acid bacteria from kuruma shrimp (Marsupenaeus japonicas) intestine and assessment of immunomodulatory role of a selected strain as probiotic. Mar Biotechnol (NY) 16(2):181–192

    CAS  Article  Google Scholar 

  • Meziti A, Kormas KA (2013) Comparison of the Norway lobster (Nephrops norvegicus) gut bacterial communities using 16S rDNA clone libraries and pyrosequencing. Anaerobe 23:9–11

    CAS  Article  PubMed  Google Scholar 

  • Moran NA, Yun Y (2015) Experimental replacement of an obligate insect symbiont. Proc Natl Acad Sci U S A 112:2093–2096

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Nordling D, Andersson M, Zohari S, Lars G (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc Biol Sci 265:1291–1298

    PubMed Central  Article  Google Scholar 

  • Prayitno SB, Sarwan, Sarjito (2015) The diversity of gut bacteria associated with Milkfish (Chanos chanos Forsksal) from Northern Coast of Central Java, Indonesia. Procedia Environ Sci 23:375–384

    Article  Google Scholar 

  • Rapala J, Berg KA, Lyra C, Niemi RM, Manz W, Suomalainen S, Paulin L, Lahti K (2005) Paucibacter toxinivorans gen. nov., sp. nov., a bacterium that degrades cyclic cyanobacterial hepatotoxins microcystins and nodularin. Int J Syst Evol Microbiol 55:1563–1568

    CAS  Article  PubMed  Google Scholar 

  • Renz H, Brandtzaeg P, Hornef M (2011) The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat Rev Immunol 12:9–23

    Article  PubMed  Google Scholar 

  • Rungrassamee W, Klanchui A, Chaiyapechara S, Maibunkaew S, Tangphatsornruang 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Shakibazadeh S, Saad C, Christianus A, Kamarudin M, Sijam K, Nor Shamsudin M, Neela V (2009) Bacteria flora associated with different body parts of hatchery reared juvenile Penaeus monodon, tanks water and sediment. Ann Microbiol 59:425–430

    Article  Google Scholar 

  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031

    Article  PubMed  Google Scholar 

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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Wang Y, Brune A, Zimmer M (2007b) Bacterial symbionts in the hepatopancreas of isopods: diversity and environmental transmission. FEMS Microbiol Ecol 61:141–152

    CAS  Article  PubMed  Google Scholar 

  • Wang C-z, Lin G-r, Yan T, Zheng Z-p, Chen B, F-l S (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 

  • Zhang M, Sun Y, Chen K, Yu N, Zhou Z, Chen L, Du Z, Li E (2014) Characterization of the intestinal microbiota in Pacific white shrimp, Litopenaeus vannamei, fed diets with different lipid sources. Aquaculture 434:449–455

    CAS  Article  Google Scholar 

  • Zhong J, Jasinskas A, Barbour AG (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS One 2:e405

    PubMed Central  Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a CRF grant (C4024-14G) from the Research Grants Council, Hong Kong Special Administrative Region, China, and grants from The Chinese University of Hong Kong.

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Author notes

  1. Patrick Tik Wan Law

    Present address: The Nethersole School of Nursing, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR

Affiliations

  1. School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR

    Man Kit Cheung, Patrick Tik Wan Law & Hoi Shan Kwan

  2. Simon F.S. Li Marine Science Laboratory, School of Life Sciences, Centre for Soybean Research, Partner State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR

    Ho Yin Yip, Wenyan Nong & Jerome Ho Lam Hui

  3. Simon F.S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong SAR

    Ka Hou Chu

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  1. Man Kit Cheung
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Correspondence to Jerome Ho Lam Hui.

Additional information

Data Deposition

Data has been deposited in NCBI Sequence Read Archive (Accession number SRR1735538).

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Figure S1

PCoA plots built using unweighted UniFrac distances. In the left panel, samples were colored according to the sampling position; in the right panel, samples were colored according to the ovarian maturation stage. (PPTX 347 kb)

Figure S2

PCoA plots built using weighted UniFrac distances. In the left panel, samples were colored according to the sampling position; in the right panel, samples were colored according to the ovarian maturation stage. (PPTX 394 kb)

Figure S3

Relative abundance of major bacterial genera recovered in the gut and hepatopancreas samples. Only genera with >1 % average relative abundance were shown here. See Table 1 for abbreviations of samples. (PPTX 104 kb)

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Cheung, M.K., Yip, H.Y., Nong, W. et al. 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, 811–819 (2015). https://doi.org/10.1007/s10126-015-9662-8

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  • DOI: https://doi.org/10.1007/s10126-015-9662-8

Keywords

  • Crustacean
  • Shrimp
  • Hepatopancreas
  • Gut
  • Ion Torrent
  • Gonad development
  • Microbiota
  • Evolution