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Contrasting Ecological Processes and Functional Compositions Between Intestinal Bacterial Community in Healthy and Diseased Shrimp

Microbial Ecology volume 72, pages 975–985 (2016)Cite this article

Abstract

Intestinal bacterial communities play a pivotal role in promoting host health; therefore, the disruption of intestinal bacterial homeostasis could result in disease. However, the effect of the occurrences of disease on intestinal bacterial community assembly remains unclear. To address this gap, we compared the multifaceted ecological differences in maintaining intestinal bacterial community assembly between healthy and diseased shrimps. The neutral model analysis shows that the relative importance of neutral processes decreases when disease occurs. This pattern is further corroborated by the ecosphere null model, revealing that the bacterial community assembly of diseased samples is dominated by stochastic processes. In addition, the occurrence of shrimp disease reduces the complexity and cooperative activities of species-to-species interactions. The keystone taxa affiliated with Alphaproteobacteria and Actinobacteria in healthy shrimp gut shift to Gammaproteobacteria species in diseased shrimp. Changes in intestinal bacterial communities significantly alter biological functions in shrimp. Within a given metabolic pathway, the pattern of enrichment or decrease between healthy and deceased shrimp is correlated with its functional effects. We propose that stressed shrimp are more prone to invasion by alien strains (evidenced by more stochastic assembly and higher migration rate in diseased shrimp), which, in turn, disrupts the cooperative activity among resident species. These findings greatly aid our understanding of the underlying mechanisms that govern shrimp intestinal community assembly between health statuses.

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References

  1. De Schryver P, Vadstein O (2014) Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME J 8:2360–2368

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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 Biotech 99:6911–6919

    CAS  Article  Google Scholar 

  3. 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. Fisheries Sci 80:1001–1007

    CAS  Article  Google Scholar 

  4. Stecher B, Chaffron S, Käppeli R, Hapfelmeier S, Freedrich S, Weber TC, Kirundi J, Suar M, McCoy KD, von Mering C (2010) Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6:e1000711

    Article  PubMed  PubMed Central  Google Scholar 

  5. Thitamadee S, Prachumwat A, Srisala J, Jaroenlak P, Salachan PV, Sritunyalucksana K, Flegel TW, Itsathitphaisarn O (2016) Review of current disease threats for cultivated penaeid shrimp in Asia. Aquaculture 452:69–87

    Article  Google Scholar 

  6. 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 

  7. Tzeng TD, Pao YY, Chen PC, Weng CH, Wen DJ, Wang D (2015) Effects of host phylogeny and habitats on gut microbiomes of oriental river prawn (Macrobrachium nipponense). Plos One 10:e0132860

    Article  PubMed  PubMed Central  Google Scholar 

  8. Sullam KE, Essinger SD, Lozupone CA, O’Connor MP, Rosen GL, Knight R, Kilham SS, Russell JA (2012) Environmental and ecological factors that shape the gut bacterial communities of fish: a meta‐analysis. Mol Ecol 21:3363–3378

    Article  PubMed  Google Scholar 

  9. Schmidt VT, Smith KF, Melvin DW, Amaral‐Zettler LA (2015) Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol Ecol 24:2537–2550

    Article  PubMed  Google Scholar 

  10. Giatsis C, Sipkema D, Smidt H, Verreth J, Verdegem M (2014) The colonization dynamics of the gut microbiota in tilapia larvae. PLoS One 9:e103641

    Article  PubMed  PubMed Central  Google Scholar 

  11. 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  Article  PubMed  Google Scholar 

  12. Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611

    Article  Google Scholar 

  13. Pérez T, Balcázar J, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz J (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360

    Article  PubMed  Google Scholar 

  14. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J (2010) Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol 59:199–211

    Article  PubMed  Google Scholar 

  15. Li CC, Chen JC (2009) The immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus under low and high pH stress. Fish Shellfish Immun 25:701–709

    CAS  Article  Google Scholar 

  16. Burns AR, Stephens WZ, Stagaman K, Wong S, Rawls JF, Guillemin K, Bohannan BJ (2016) Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J 10:655–664

    Article  PubMed  Google Scholar 

  17. Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, 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. doi:10.1111/1462-2920.13365

    Google Scholar 

  18. Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3:417

    Article  PubMed  PubMed Central  Google Scholar 

  19. Chase JM, Kraft NJ, Smith KG, Vellend M, Inouye BD (2011) Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2:art24

    Article  Google Scholar 

  20. Xiong J, Chen H, Hu C, Ye X, Kong D, Zhang D (2015) Evidence of bacterioplankton community adaptation in response to long-term mariculture disturbance. Sci Rep 5:15274

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos T R Soci B 366:2351–2363

    Article  Google Scholar 

  22. Loudon AH, Venkataraman A, Vantreuren W, Woodhams D, Parfrey LW, Mckenzie V, Knight R, Schmidt T, Harris R (2016) Vertebrate hosts as islands: dynamics of selection, immigration, loss, persistence, and potential function of bacteria on Salamander skin. Front Microbiol 7:333

    Article  PubMed  PubMed Central  Google Scholar 

  23. Vanwonterghem I, Jensen PD, Dennis PG, Hugenholtz P, Rabaey K, Tyson GW (2014) Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME J 8:2015–2018

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Lepori F, Malmqvist B (2009) Deterministic control on community assembly peaks at intermediate levels of disturbance. Oikos 118:471–479

    Article  Google Scholar 

  25. 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

    CAS  Article  PubMed  Google Scholar 

  26. Fan L, Wang A, Miao Y, Liao S, Ye C, Lin Q (2016) Comparative proteomic identification of the hepatopancreas response to cold stress in white shrimp, Litopenaeus vannamei. Aquaculture 202:651–654

    Google Scholar 

  27. Allison SD, Martiny JB (2008) Resistance, resilience, and redundancy in microbial communities. Proc Nat Acad Sci USA 105:11512–11519

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Mcfrederick QS, Mueller UG, James RR (2014) Interactions between fungi and bacteria influence microbial community structure in the Megachile rotundata larval gut. P Roy Soc B-Biol Sci 281:85–94

    Article  Google Scholar 

  29. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

    CAS  Article  PubMed  Google Scholar 

  30. Deng Y, Zhang P, Qin Y, Tu Q, Yang Y, He Z, Schadt CW, Zhou J (2016) Network succession reveals the importance of competition in response to emulsified vegetable oil amendment for uranium bioremediation. Environ Microbiol 18:205–218

    CAS  Article  PubMed  Google Scholar 

  31. Zhang P, Wu W-M, Van Nostrand JD, Deng Y, He Z, Gihring T, Zhang G, Schadt CW, Watson D, Jardine P (2015) Dynamic succession of groundwater functional microbial communities in response to emulsified vegetable oil amendment during sustained in situ U (VI) reduction. Appl Environ Microbiol 81:4164–4172

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

  34. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust Ecol 18:117–143

    Article  Google Scholar 

  35. Wu J, Xiong J, Hu C, Shi Y, Wang K, Zhang D (2015) Temperature sensitivity of soil bacterial community along contrasting warming gradient. Appl Soil Ecol 94:40–48

    Article  Google Scholar 

  36. Xiong J, Fei P, Sun H, Xian X, Chu H (2014) Divergent responses of soil fungi functional groups to short-term warming. Microb Ecol 68:708–715

    CAS  Article  PubMed  Google Scholar 

  37. Sloan WT, Mary L, Stephen W, Head IM, Sean N, Curtis TP (2006) Quantifying the roles of immigration and chance in shaping prokaryote community structure. Environ Microbiol 8:732–740

    Article  PubMed  Google Scholar 

  38. Elzhov TV, Mullen KM, Spiess AN, Bolker B (2013) minpack.lm: R interface to the Levenberg-Marquardt nonlinear least-squares algorithm found in MINPACK, plus support for bounds. R package version 11-8 http://CRANR-project.org/package=minpacklm.

  39. DasGupta A, Cai TT, Brown LD (2001) Interval estimation for a binomial proportion. Stat Sci 16:101–133

    Article  Google Scholar 

  40. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0

    Google Scholar 

  41. Östman Ö, Drakare S, Kritzberg ES, Langenheder S, Logue JB, Lindström ES (2010) Regional invariance among microbial communities. Ecol Lett 13:118–127

    Article  PubMed  Google Scholar 

  42. Sloan WT, Woodcock S, Lunn M, Head IM, Curtis TP (2007) Modeling taxa-abundance distributions in microbial communities using environmental sequence data. Microb Ecol 53:443–455

    Article  PubMed  Google Scholar 

  43. Kraft NJB, Comita LS, Chase JM, Sanders NJ, Swenson NG, Crist TO, Stegen JC, Mark V, Brad B, Anderson MJ (2011) Disentangling the drivers of β diversity along latitudinal and elevational gradients. Science 333:1755–1758

    CAS  Article  PubMed  Google Scholar 

  44. Zhou J, Deng Y, Zhang P, Xue K, Liang Y, Van Nostrand JD, Yang Y, He Z, Wu L, Stahl DA, Hazen TC, Tiedje JM, Arkin AP (2014) Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proc Nat Acad Sci USA 111:836–845

    Article  Google Scholar 

  45. Deng Y, Jiang Y, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113

    Article  PubMed  PubMed Central  Google Scholar 

  46. Newman MEJ (2003) The structure and function of complex networks. SIAM Rev 45:167–256

    Article  Google Scholar 

  47. Shannon P, Markiel A, Ozier O, Baliga NS, Wang J, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 14:e1003531

    Article  Google Scholar 

  49. Williams RJ, Howe A, Hofmockel KS (2014) Demonstrating microbial co-occurrence pattern analyses within and between ecosystems. Front Microbiol 5:358

    Article  PubMed  PubMed Central  Google Scholar 

  50. Montoya JM, Pimm SL, Solé RV (2006) Ecological networks and their fragility. Nature 442:259–264

    CAS  Article  PubMed  Google Scholar 

  51. Jiang L, Morin PJ (2004) Productivity gradients cause positive diversity-invasibility relationships in microbial communities. J Appl Psychol 7:1047–1057

    Google Scholar 

  52. De Roy K, Marzorati M, Negroni A, Thas O, Balloi A, Fava F, Verstraete W, Daffonchio D, Boon N (2013) Environmental conditions and community evenness determine the outcome of biological invasion. Nat Commun 4:1383

    Article  PubMed  Google Scholar 

  53. Bailey MT (2012) The contributing role of the intestinal microbiota in stressor-induced increases in susceptibility to enteric infection and systemic immunomodulation. Horm Behav 62:286–294

    CAS  Article  PubMed  Google Scholar 

  54. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, Finlay BB (2008) Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 76:4726–4736

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Ninawe A, Selvin J (2009) Probiotics in shrimp aquaculture: avenues and challenges. Crit Rev Microbiol 35:43–66

    CAS  Article  PubMed  Google Scholar 

  56. Mugnier C, Justou C, Lemonnier H, Patrois J, Ansquer D, Goarant C, Lecoz JR (2013) Biological, physiological, immunological and nutritional assessment of farm-reared Litopenaeus stylirostris shrimp affected or unaffected by vibriosis. Aquaculture 388–391:105–114

    Article  Google Scholar 

  57. Scheuring I, Yu DW (2012) How to assemble a beneficial microbiome in three easy steps. Ecol Lett 15:1300–1307

    Article  PubMed  PubMed Central  Google Scholar 

  58. Wen C, Xue M, Liang H, Zhou S (2014) Evaluating the potential of marine Bacteriovorax sp. DA5 as a biocontrol agent against vibriosis in Litopenaeus vannamei larvae. Vet Microbiol 173:84–91

    Article  PubMed  Google Scholar 

  59. Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199

    CAS  Article  PubMed  Google Scholar 

  60. Mahajan GB, Balachandran L (2012) Antibacterial agents from actinomycetes—a review. Front Biosci 4:240–253

    Article  Google Scholar 

  61. Stecher B, Hardt WD (2011) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 14:82–91

    CAS  Article  PubMed  Google Scholar 

  62. Moya A, Ferrer M (2016) Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol 24:402–413

    CAS  Article  PubMed  Google Scholar 

  63. Knelman JE, Nemergut DR (2014) Changes in community assembly may shift the relationship between biodiversity and ecosystem function. Front Microbiol 5:424

    Article  PubMed  PubMed Central  Google Scholar 

  64. Claud EC, Keegan KP, Brulc JM, Lu L, Bartels D, Glass E, Chang EB, Meyer F, Antonopoulos DA (2013) Bacterial community structure and functional contributions to emergence of health or necrotizing enterocolitis in preterm infants. Microbiome 1:20

    Article  PubMed  PubMed Central  Google Scholar 

  65. Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160

    CAS  Article  PubMed  Google Scholar 

  66. Vigne JD, Lefèvre C, Patoumathis M (2013) Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration. J Clin Microbiol 51:849–856

    Article  Google Scholar 

  67. Kline KA, Fälker S, Dahlberg S, Normark S, Henriques-Normark B (2009) Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5:580–592

    CAS  Article  PubMed  Google Scholar 

  68. Settembre C, Fraldi A, Medina DL, Ballabio A (2013) Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat Rev Mol Cell Biol 14:283–296

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Guimera R, Sales-Pardo M, Amaral LA (2007) Classes of complex networks defined by role-to-role connectivity profiles. Nat Physcis 3:63–69

    CAS  Article  Google Scholar 

  70. Newman ME (2006) Modularity and community structure in networks. Proc Nat Acad Sci USA 103:8577–8582

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Zhejiang Province Public Welfare Technology Application Research Project (2016C32063); the Spark Program of China (2015GA701024); the Open Fund of Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography (HY201601); and the KC Wong Magna Fund of Ningbo University.

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Affiliations

  1. School of Marine Sciences, Ningbo University, Ningbo, 315211, China

    Jinyong Zhu, Wenfang Dai, Qiongfen Qiu, Jinjie Zhang & Jinbo Xiong

  2. Collaborative Innovation Center for Zhejiang Marine High-Efficiency and Healthy Aquaculture, Ningbo, 315211, China

    Wenfang Dai & Jinbo Xiong

  3. Key Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State of Oceanic Administration, Xiamen, 361006, China

    Chunming Dong

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  1. Jinyong Zhu
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Correspondence to Jinbo Xiong.

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Zhu, J., Dai, W., Qiu, Q. et al. Contrasting Ecological Processes and Functional Compositions Between Intestinal Bacterial Community in Healthy and Diseased Shrimp. Microb Ecol 72, 975–985 (2016). https://doi.org/10.1007/s00248-016-0831-8

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Keywords

  • Shrimp intestinal community
  • Health status
  • Ecological process
  • Species-to-species interactions
  • Functional composition