Journal of Microbiology and Biotechnology

  • 제28권6호
  • /
  • Pages.946-956
  • /
  • 2018
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Insights into the Gut Microbiota of Freshwater Shrimp and Its Associations with the Surrounding Microbiota and Environmental Factors

  • Zhao, Yanting (State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University) ;
  • Duan, Cuilan (Fisheries Technology Extension Center of Jiangsu Province) ;
  • Zhang, Xu-xiang (State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University) ;
  • Chen, Huangen (Fisheries Technology Extension Center of Jiangsu Province) ;
  • Ren, Hongqiang (State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University) ;
  • Yin, Ying (State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University) ;
  • Ye, Lin (State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University)
  • 투고 : 2017.09.26
  • 심사 : 2018.03.08
  • 발행 : 2018.06.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

The gut microbiota of aquatic animals plays a crucial role in host health through nutrient acquisition and outcompetition of pathogens. In this study, on the basis of the high-throughput sequencing of 16S rRNA gene amplicons, we examined the bacterial communities in the gut of freshwater shrimp (Macrobrachium nipponense) and in their living environments (sediment and pond water) and analyzed the effects of abiotic and biotic factors on the shrimp gut bacterial communities. High bacterial heterogeneity was observed in the freshwater shrimp gut samples, and the result indicated that both the surrounding bacterial community and water quality factors (particularly dissolved oxygen and temperature) could affect the shrimp gut bacterial community. Despite the observed heterogeneity, 57 genera, constituting 38-99% of the total genera in each of the 40 shrimp gut samples, were identified as the main bacterial population in the gut of M. nipponense. In addition, a high diversity and abundance of lactic acid bacteria (26 genera), which could play significant roles in the digestion process in shrimp, were observed in the shrimp gut samples. Overall, this study provides insights into the gut bacterial communities of freshwater shrimp and basic information for shrimp farming regarding the application of probiotics and disease prevention.

키워드

참고문헌

  1. Backhed F. 2011. Programming of host metabolism by the gut microbiota. Ann. Nutr. Metab. 58: 44-52. https://doi.org/10.1159/000328042
  2. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. 2008. Evolution of mammals and their gut microbes. Science 320: 1647-1651. https://doi.org/10.1126/science.1155725
  3. Angelakis E, Armougom F, Million M, Raoult D. 2012. The relationship between gut microbiota and weight gain in humans. Future Microbiol. 7: 91-109. https://doi.org/10.2217/fmb.11.142
  4. Khan I, Yasir M, Azhar EI, Kumosani T, Barbour EK, Bibi F, et al. 2014. Implication of gut microbiota in human health. CNS Neurol. Disord. Drug Targets 13: 1325-1333. https://doi.org/10.2174/1871527313666141023153506
  5. Schnabl B, Brenner DA. 2014. Interactions between the intestinal microbiome and liver diseases. Gastroenterology 146: 1513-1524. https://doi.org/10.1053/j.gastro.2014.01.020
  6. Grigorescu I, Dumitrascu DL. 2016. Implication of gut microbiota in diabetes mellitus and obesity. Acta Endocrinol. (Bucharest) 12: 206-214. https://doi.org/10.4183/aeb.2016.206
  7. Moeller AH, Li Y, Ngole EM, Ahuka-Mundeke S, Lonsdorf EV, Pusey AE, et al. 2014. Rapid changes in the gut microbiome during human evolution. Proc. Natl. Acad. Sci. USA 111: 16431-16435. https://doi.org/10.1073/pnas.1419136111
  8. Jacobs J, Braun J. 2014. Host genes and their effect on the intestinal microbiome garden. Genome Med. 6: 119. https://doi.org/10.1186/s13073-014-0119-x
  9. Konya T, Koster B, Maughan H, Escobar M, Azad MB, Guttman DS, et al. 2014. Associations between bacterial communities of house dust and infant gut. Environ. Res. 131: 25-30. https://doi.org/10.1016/j.envres.2014.02.005
  10. Sullam KE, Essinger SD, Lozupone CA, O'Connor MP, Rosen GL, Knight R, et al. 2012. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol. Ecol. 21: 3363-3378. https://doi.org/10.1111/j.1365-294X.2012.05552.x
  11. Kohl KD, Yahn J. 2016. Effects of environmental temperature on the gut microbial communities of tadpoles. Environ. Microbiol. 18: 1561-1565. https://doi.org/10.1111/1462-2920.13255
  12. Costello EK, Stagaman K, Dethlefsen L, Bohannan BJM, Relman DA. 2012. The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255-1262. https://doi.org/10.1126/science.1224203
  13. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10: 497-506. https://doi.org/10.1038/nrmicro2795
  14. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. 2006. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4: 102-112. https://doi.org/10.1038/nrmicro1341
  15. Yan Q, Li J, Yu Y, Wang J, He Z, Van Nostrand JD, et al. 2016. Environmental filtering decreases with fish development for the assembly of gut microbiota. Environ. Microbiol. 18: 4739-4754. https://doi.org/10.1111/1462-2920.13365
  16. Gibson DJ, Ely JS, Collins SL. 1999. The core-satellite species hypothesis provides a theoretical basis for Grime's classification of dominant, subordinate, and transient species. J. Ecol. 87: 1064-1067. https://doi.org/10.1046/j.1365-2745.1999.00424.x
  17. Cariveau DP, Powell JE, Koch H, Winfree R, Moran NA. 2014. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J. 8: 2369-2379. https://doi.org/10.1038/ismej.2014.68
  18. Otani S, Mikaelyan A, Nobre T, Hansen LH, Kone NGA, Sorensen SJ, et al. 2014. Identifying the core microbial community in the gut of fungus-growing termites. Mol. Ecol. 23: 4631-4644. https://doi.org/10.1111/mec.12874
  19. Dishaw LJ, Flores-Torres J, Lax S, Gemayel K, Leigh B, Melillo D, et al. 2014. The gut of geographically disparate Ciona intestinalis harbors a core microbiota. PLoS One 9: e93386. https://doi.org/10.1371/journal.pone.0093386
  20. Wong ACN, Chaston JM, Douglas AE. 2013. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 7: 1922-1932. https://doi.org/10.1038/ismej.2013.86
  21. Greenhalgh K, Meyer KM, Aagaard KM, Wilmes P. 2016. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ. Microbiol. 18: 2103-2116. https://doi.org/10.1111/1462-2920.13318
  22. Engel P, Moran NA. 2013. The gut microbiota of insects - diversity in structure and function. FEMS Microbiol. Rev. 37: 699-735. https://doi.org/10.1111/1574-6976.12025
  23. Balcazar JL, de Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Muzquiz JL. 2006. The role of probiotics in aquaculture. Vet. Microbiol. 114: 173-186. https://doi.org/10.1016/j.vetmic.2006.01.009
  24. Liu H, Liu M, Wang B, Jiang K, Jiang S, Sun S, et al. 2010. PCR-DGGE analysis of intestinal bacteria and effect of Bacillus spp. on intestinal microbial diversity in kuruma shrimp (Marsupenaeus japonicus). Chin. J. Oceanol. Limnol. 28: 808-814. https://doi.org/10.1007/s00343-010-9101-7
  25. 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. https://doi.org/10.1371/journal.pone.0091853
  26. Rahman NMA, Fu HT, Sun SM, Qiao H, Jin S, Bai HK, et al. 2016. Molecular cloning and expression pattern of oriental river prawn (Macrobrachium nipponense) nitric oxide synthase. Genet. Mol. Res. 15: DOI: 10.4238/gmr.15038541.
  27. Tzeng T-D, Pao Y-Y, Chen P-C, Weng FC-H, Jean WD, Wang D. 2015. Effects of host phylogeny and habitats on gut microbiomes of oriental river prawn (Macrobrachium nipponense). PLoS One 10: e0132860. https://doi.org/10.1371/journal.pone.0132860
  28. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541. https://doi.org/10.1128/AEM.01541-09
  29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7: 335-336. https://doi.org/10.1038/nmeth.f.303
  30. 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: 5261-5267. https://doi.org/10.1128/AEM.00062-07
  31. Jiang X-T, Peng X, Deng G-H, Sheng H-F, Wang Y, Zhou H-W, et al. 2013. Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb. Ecol. 66: 96-104. https://doi.org/10.1007/s00248-013-0238-8
  32. Rungrassamee W, Klanchui A, Chaiyapechara S, Maibunkaew S, Tangphatsornruang S, Jiravanichpaisal P, et al. 2013. Bacterial population in intestines of the black tiger shrimp (Penaeus monodon) under different growth stages. PLoS One 8: e60802. https://doi.org/10.1371/journal.pone.0060802
  33. Kim D-U, Lee H, Kim H, Kim S-G, Ka J-O. 2016. Dongia soli sp. nov., isolated from soil from Dokdo, Korea. Antonie Van Leeuwenhoek 109: 1397-1402. https://doi.org/10.1007/s10482-016-0738-x
  34. Baik KS, Hwang YM, Choi J-S, Kwon J, Seong CN. 2013. Dongia rigui sp. nov., isolated from freshwater of a large wetland in Korea. Antonie Van Leeuwenhoek 104: 1143-1150. https://doi.org/10.1007/s10482-013-0036-9
  35. Rahalkar M, Bahulikar RA, Deutzmann JS, Kroth PG, Schink B. 2012. Elstera litoralis gen. nov., sp nov., isolated from stone biofilms of Lake Constance, Germany. Int. J. Syst. Evol. Microbiol. 62: 1750-1754. https://doi.org/10.1099/ijs.0.026609-0
  36. Ye L, Amberg J, Chapman D, Gaikowski M, Liu W-T. 2014. Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish. ISME J. 8: 541-551. https://doi.org/10.1038/ismej.2013.181
  37. Prewitt L, Kang Y, Kakumanu ML, Williams M. 2014. Fungal and bacterial community succession differs for three wood types during decay in a forest soil. Microb. Ecol. 68: 212-221. https://doi.org/10.1007/s00248-014-0396-3
  38. Bletz MC, Goedbloed DJ, Sanchez E, Reinhardt T, Tebbe CC, Bhuju S, et al. 2016. Amphibian gut microbiota shifts differentially in community structure but converges on habitat-specific predicted functions. Nat. Commun. 7: 13699. https://doi.org/10.1038/ncomms13699
  39. Staley C, Gould TJ, Wang P, Phillips J, Cotner JB, Sadowsky MJ. 2015. Species sorting and seasonal dynamics primarily shape bacterial communities in the Upper Mississippi River. Sci. Total Environ. 505: 435-445. https://doi.org/10.1016/j.scitotenv.2014.10.012
  40. De Schryver P, Vadstein O. 2014. Ecological theory as a foundation to control pathogenic invasion in aquaculture. ISME J. 8: 2360-2368. https://doi.org/10.1038/ismej.2014.84
  41. Berg M, Stenuit B, Ho J, Wang A, Parke C, Knight M, et al. 2016. Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. ISME J. 10: 1998-2009. https://doi.org/10.1038/ismej.2015.253
  42. Dec M, Puchalski A, Nowaczek A, Wernicki A. 2016. Antimicrobial activity of Lactobacillus strains of chicken origin against bacterial pathogens. Int. Microbiol. 19: 57-67.
  43. Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, et al. 2016. The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci. Rep. 6: 24340. https://doi.org/10.1038/srep24340
  44. Ray AK, Ghosh K, Ringo E. 2012. Enzyme-producing bacteria isolated from fish gut: a review. Aquac. Nutr. 18: 465-492. https://doi.org/10.1111/j.1365-2095.2012.00943.x
  45. Xu J, Mahowald MA, Ley RE, Lozupone CA, Hamady M, Martens EC, et al. 2007. Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 5: 1574-1586.
  46. Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF, Hossain MS, et al. 2016. Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major. Fish Shellfish Immunol. 49: 275-285. https://doi.org/10.1016/j.fsi.2015.12.047
  47. Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, et al. 2011. Microbial manipulations to improve fish health and production - a Mediterranean perspective. Fish Shellfish Immunol. 30: 1-16. https://doi.org/10.1016/j.fsi.2010.08.009
  48. Geng X, Dong XH, Tan BP, Yang QH, Chi SY, Liu HY, et al. 2012. Effects of dietary probiotic on the growth performance, non-specific immunity and disease resistance of cobia, Rachycentron canadum. Aquac. Nutr. 18: 46-55. https://doi.org/10.1111/j.1365-2095.2011.00875.x
  49. Kuda T, Masuko Y, Kawahara M, Kondo S, Nemoto M, Nakata T, et al. 2016. Bile acid-lowering properties of Lactobacillus plantarum Sanriku-SU3 isolated from Japanese surfperch fish. Food Biosci. 14: 41-46. https://doi.org/10.1016/j.fbio.2016.02.004
  50. Kuda T, Noguchi Y, Ono M, Takahashi H, Kimura B, Kamita R, et al. 2014. In vitro evaluation of the fermentative, antioxidant, and anti-inflammation properties of Lactococcus lactis subsp. lactis BF3 and Leuconostoc mesenteroides subsp. mesenteroides BF7 isolated from Oncorhynchus keta intestines in Rausu, Japan. J. Funct. Foods 11: 269-277. https://doi.org/10.1016/j.jff.2014.09.017
  51. Russo P, Iturria I, Luz Mohedano M, Caggianiello G, Rainieri S, Fiocco D, et al. 2015. Zebrafish gut colonization by mCherry-labelled lactic acid bacteria. Appl. Microbiol. Biotechnol. 99: 3479-3490. https://doi.org/10.1007/s00253-014-6351-x
  52. Liu J, Yan Q, Luo F, Shang D, Wu D, Zhang H, et al. 2015. Acute cholecystitis associated with infection of Enterobacteriaceae from gut microbiota. Clin. Microbiol. Infect. 21: 851.e19.
  53. Cabello FC. 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8: 1137-1144. https://doi.org/10.1111/j.1462-2920.2006.01054.x
  54. Tang Y, Tao P, Tan J, Mu H, Peng L, Yang D, et al. 2014. Identification of bacterial community composition in freshwater aquaculture system farming of Litopenaeus vannamei reveals distinct temperature-driven patterns. Int. J. Mol. Sci. 15: 13663-13680. https://doi.org/10.3390/ijms150813663
  55. Montiel Quezel-Guerraz N, Marin Arriaza M, Carrillo Avila JA, Sanchez-Yebra Romera WE, Martinez-Lirola MJ, Indal TBG. 2010. Evaluation of the Speed-oligo (R) Mycobacteria assay for identification of Mycobacterium spp. from fresh liquid and solid cultures of human clinical samples. Diagn. Microbiol. Infect. Dis. 68: 123-131. https://doi.org/10.1016/j.diagmicrobio.2010.06.006
  56. Abass NA, Suleiman KM, El Jalii IM. 2010. Differentiation of clinical Mycobacterium tuberculosis complex isolates by their GyrB polymorphism. Indian J. Med. Microbiol. 28: 26-29. https://doi.org/10.4103/0255-0857.58724
  57. Manfredi R, Nanetti A, Ferri M, Mastroianni A, Coronado OV, Chiodo F. 1999. Flavobacterium spp. organisms as opportunistic bacterial pathogens during advanced HIV disease. J. Infect. 39: 146-152. https://doi.org/10.1016/S0163-4453(99)90007-5
  58. Toranzo AE, Magarinos B, Romalde JL. 2005. A review of the main bacterial fish diseases in mariculture systems. Aquaculture 246: 37-61. https://doi.org/10.1016/j.aquaculture.2005.01.002
  59. Tall A, Teillon A, Boisset C, Delesmont R, Touron-Bodilis A, Hervio-Heath D. 2012. Real-time PCR optimization to identify environmental Vibrio spp. strains. J. Appl. Microbiol. 113: 361-372. https://doi.org/10.1111/j.1365-2672.2012.05350.x
  60. 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. https://doi.org/10.1016/j.jip.2015.11.004
  61. 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. https://doi.org/10.1007/s00253-016-7679-1
  62. Ringo E, Olsen RE, Gifstad TO, Dalmo RA, Amlund H, Hemre GI, et al. 2010. Prebiotics in aquaculture: a review. Aquac. Nutr. 16: 117-136. https://doi.org/10.1111/j.1365-2095.2009.00731.x
  63. Attramadal KJK, Thi My Hanh T, Bakke I, Skjermo J, Olsen Y, Vadstein O. 2014. RAS and microbial maturation as tools for K-selection of microbial communities improve survival in cod larvae. Aquaculture 432: 483-490. https://doi.org/10.1016/j.aquaculture.2014.05.052
  64. Attramadal KJK, Salvesen I, Xue R, Oie G, Storseth TR, Vadstein O, et al. 2012. Recirculation as a possible microbial control strategy in the production of marine larvae. Aquac. Eng. 46: 27-39. https://doi.org/10.1016/j.aquaeng.2011.10.003

피인용 문헌

  1. Dynamics of the gut microbiota in developmental stages of Litopenaeus vannamei reveal its association with body weight vol.9, pp.None, 2018, https://doi.org/10.1038/s41598-018-37042-3
  2. Assessment of the Dynamics of Microbial Community Associated with Tetraselmis suecica Culture under Different LED Lights Using Next-Generation Sequencing vol.29, pp.12, 2018, https://doi.org/10.4014/jmb.1910.10046
  3. BALOs Improved Gut Microbiota Health in Postlarval Shrimp ( Litopenaeus vannamei ) After Being Subjected to Salinity Reduction Treatment vol.11, pp.None, 2018, https://doi.org/10.3389/fmicb.2020.01296
  4. Combining proteogenomics and metaproteomics for deep taxonomic and functional characterization of microbiomes from a non-sequenced host vol.6, pp.None, 2020, https://doi.org/10.1038/s41522-020-0133-2
  5. Fine-scale succession patterns and assembly mechanisms of bacterial community of Litopenaeus vannamei larvae across the developmental cycle vol.8, pp.1, 2018, https://doi.org/10.1186/s40168-020-00879-w
  6. Microbial diversity and ecology of crustaceans: influencing factors and future perspectives vol.39, pp.None, 2018, https://doi.org/10.1016/j.cofs.2021.01.001
  7. Dissolution-based uptake of CeO2 nanoparticles by freshwater shrimp - a dual-radiolabelling study of the fate of anthropogenic cerium in water organisms vol.8, pp.7, 2018, https://doi.org/10.1039/d1en00264c