Microbiota assemblages of water, sediment, and intestine and their associations with environmental factors and shrimp physiological health

Huang, Fei; Pan, Luqing; Song, Mengsi; Tian, Changcheng; Gao, Shuo

doi:10.1007/s00253-018-9229-5

Environmental biotechnology
Published: 23 July 2018

Microbiota assemblages of water, sediment, and intestine and their associations with environmental factors and shrimp physiological health

Fei Huang¹,
Luqing Pan¹^nAff2,
Mengsi Song¹,
Changcheng Tian¹ &
Shuo Gao¹

Applied Microbiology and Biotechnology volume 102, pages 8585–8598 (2018)Cite this article

1606 Accesses
48 Citations
1 Altmetric
Metrics details

Abstract

Microorganisms play crucial roles in nutrient cycling, water quality maintenance, and farmed animal health. Increasing evidences have revealed a close association between unstable microbial environments and disease occurrences in aquaculture. Thereupon, we used high-throughput sequencing technology to comprehensively compare the bacterial communities of water, sediment, and intestine in mariculture ponds at the middle and late stages of Litopenaeus vannamei farming and analyzed whether changes of their microbiota assemblages were associated with environmental factors and shrimp physiological health. Results showed that bacterial community structures were significantly distinct among water, sediment, and intestine; meanwhile, the relative abundances of intestinal dominant taxa were significantly changed between different rearing stages. Compared with intestine and water, shrimp intestine and sediment had a similar profile of the dominant bacterial genera by cluster analysis, and the observed species, diversity indexes, and shared OTUs of bacterial communities in intestine and sediment were simultaneously increased after shrimp were farmed for 90 days. These results reflected a closer relationship between microbiotas in sediment and intestine, which was further proved by nonmetric multidimensional scaling analysis. However, bacterial communities in water, sediment, and intestine responded differently to environmental variables by redundancy and correlation analysis. More importantly, shrimp physiological parameters were closely associated with bacterial variations in the gut and/or ambient, especially the gut microbiota owning significantly high levels of predicted functional pathways involved in disease emergence. These findings may greatly add to our understanding of the microbiota characteristics of the shrimp pond ecosystem and the complex interactions among shrimp, ambient microflora, and environmental variables.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Abid A, Davies SJ, Waines P, Emery M, Castex M, Gioacchini G, Carnevali O, Bickerdike R, Romero J, Merrifield DL (2013) Dietary synbiotic application modulates Atlantic salmon (Salmo salar) intestinal microbial communities and intestinal immunity. Fish Shellfish Immunol 35:1948–1956. https://doi.org/10.1016/j.fsi.2013.09.039
CAS Article PubMed Google Scholar
Adams A (1991) Response of penaeid shrimp to exposure to Vibrio species. Fish Shellfish Immunol 1:59–70. https://doi.org/10.1016/S1050-4648(06)80020-3
Article Google Scholar
Anneke E, Lenny H, Jan S (2013) Pathogen–host–environment interplay and disease emergence. Emerg Microbes Infect 2:e5. https://doi.org/10.1038/emi.2013.5
CAS Article Google Scholar
Bakke I, Åm AL, Kolarevic J, Ytrestøyl T, Vadstein O, Attramadal KJK, Terjesen BF (2016) Microbial community dynamics in semi-commercial RAS for production of Atlantic salmon post-smolts at different salinities. Aquac Eng 78:42–49. https://doi.org/10.1016/j.aquaeng.2016.10.002
Article Google Scholar
Blancheton JP, Attramadal KJK, Michaud L, D’Orbcastel ER, Vadstein O (2013) Insight into bacterial population in aquaculture systems and its implication. Aquac Eng 53:30–39. https://doi.org/10.1016/j.aquaeng.2012.11.009
Article Google Scholar
Braak T, Smilauer P (2002) Canoco reference manual and CanoDraw for Windows user's guide: software for canonical community ordination. Ithaca NY USA
Google Scholar
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
CAS Article PubMed PubMed Central Google Scholar
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Article Google Scholar
Clemente JC, Ursell LK, Parfrey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270. https://doi.org/10.1016/j.cell.2012.01.035
CAS Article PubMed PubMed Central Google Scholar
Clescerl LS (1998) Standard methods for the examination of water and wastewater, 20th edn. APHA, Washington
Google Scholar
Cornejo-Granados F, Lopezzavala AA, Gallardobecerra L, Mendozavargas A, Sánchez F, Vichido R, Brieba LG, Viana MT, Sotelomundo RR, Ochoaleyva A (2017) Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between wild, aquacultured and AHPND/EMS outbreak conditions. Sci Rep 7:e11783. https://doi.org/10.1038/s41598-017-11805-w
CAS Article Google Scholar
Dehler CE, Secombes CJ, Martin SAM (2016) Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L). Aquaculture 467:149–157. https://doi.org/10.1016/j.aquaculture.2016.07.017
CAS Article Google Scholar
Del'Duca A, Cesar DE, Abreu PC (2015) Bacterial community of pond's water, sediment and in the guts of tilapia (Oreochromis niloticus) juveniles characterized by fluorescent in situ hybridization technique. Aquac Res 46:707–715. https://doi.org/10.1111/are.12218
Article Google Scholar
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
CAS Article PubMed PubMed Central Google Scholar
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
CAS Article PubMed Google Scholar
Fan L, Barry K, Hu G, Meng S, Song C, Qiu L, Zheng Y, Wu W, Qu J, Chen J (2017) Characterizing bacterial communities in tilapia pond surface sediment and their responses to pond differences and temporal variations. World J Microbiol Biotechnol 33:e1. https://doi.org/10.1007/s11274-016-2144-y
Article Google Scholar
Ferreira NC, Bonetti C, Seiffert WQ (2011) Hydrological and water quality indices as management tools in marine shrimp culture. Aquaculture 318:425–433. https://doi.org/10.1016/j.aquaculture.2011.05.045
Article Google Scholar
FAO (2014) The state of world fisheries and aquaculture. FAO Rome, Italy
Google Scholar
Giatsis C, Sipkema D, Smidt H, Heilig H, Benvenuti G, Verreth J, Verdegem M (2015) The impact of rearing environment on the development of gut microbiota in tilapia larvae. Sci Rep 5:e18206. https://doi.org/10.1038/srep18206
CAS Article Google Scholar
Hai NV (2015) The use of probiotics in aquaculture. J Appl Microbiol 119:917–935. https://doi.org/10.1111/jam.12886
CAS Article PubMed Google Scholar
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 47:1737–1746. https://doi.org/10.1111/are.12628
Article Google Scholar
Ingerslev HC, Strube ML, Jørgensen LVG, Dalsgaard I, Boye M, Madsen L (2014) Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 40:624–633. https://doi.org/10.1016/j.fsi.2014.08.021
CAS Article PubMed Google Scholar
Langille MG, Zaneveld J, Caporaso JG, Mcdonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
CAS Article PubMed PubMed Central Google Scholar
Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Book Google Scholar
Ling Z, Liu X, Jia X, Cheng Y, Luo Y, Li Y, Wang Y, Zhao C, Guo S, Li L (2014) Impacts of infection with different toxigenic Clostridium difficile strains on faecal microbiota in children. Sci Rep 4:e7485. https://doi.org/10.1038/srep07485
CAS Article Google Scholar
Liu H, Li Z, Tan B, Lao Y, Duan Z, Sun W, Dong X (2014) Isolation of a putative probiotic strain S12 and its effect on growth performance, non-specific immunity and disease-resistance of white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 41:300–307. https://doi.org/10.1016/j.fsi.2014.08.028
CAS Article PubMed Google Scholar
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinform 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
CAS Article Google Scholar
Mahajan GB, Balachandran L (2012) Antibacterial agents from actinomycetes—a review. Front Biosci 4:240–253. https://doi.org/10.2741/373
Article Google Scholar
Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, Blas ID, Múzquiz JL (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360. https://doi.org/10.1038/mi.2010.12
CAS Article PubMed Google Scholar
Qin Y, Hou J, Deng M, Liu Q, Wu C, Ji Y, He X (2016) Bacterial abundance and diversity in pond water supplied with different feeds. Sci Rep 6:e35232. https://doi.org/10.1038/srep35232
CAS Article Google Scholar
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219
CAS Article Google Scholar
Round JL (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323. https://doi.org/10.1038/nri2515
CAS Article PubMed PubMed Central Google Scholar
Rungrassamee W, Klanchui A, Maibunkaew S, Karoonuthaisiri N (2015) 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
CAS Article PubMed Google Scholar
Schryver PD, 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
Article PubMed PubMed Central Google Scholar
Smalley NE, Taipale S, De MP, Doronina NV, Kyrpides N, Shapiro N, Woyke T, Kalyuzhnaya MG (2015) Functional and genomic diversity of methylotrophic Rhodocyclaceae: description of Methyloversatilis discipulorum sp. nov. Int J Syst Evol Microbiol 65:2227–2233. https://doi.org/10.1099/ijs.0.000190
CAS Article PubMed Google Scholar
Soonthornchai W, Rungrassamee W, Karoonuthaisiri N, Jarayabhand P, Klinbunga S, Söderhäll K, Jiravanichpaisal P (2010) Expression of immune-related genes in the digestive organ of shrimp, Penaeus monodon, after an oral infection by Vibrio harveyi. Dev Comp Immunol 34:19–28. https://doi.org/10.1016/j.dci.2009.07.007
CAS Article PubMed Google Scholar
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. https://doi.org/10.1111/j.1365-294X.2012.05552.x
Article PubMed Google Scholar
Sun YZ, Yang HL, Ma RL, Lin WY (2010) Probiotic applications of two dominant gut Bacillus strains with antagonistic activity improved the growth performance and immune responses of grouper Epinephelus coioides. Fish Shellfish Immunol 29:803–809. https://doi.org/10.1016/j.fsi.2010.07.018
Article PubMed Google Scholar
Tassanakajon A, Somboonwiwat K, Supungul P, Tang S (2013) Discovery of immune molecules and their crucial functions in shrimp immunity. Fish Shellfish Immunol 34:954–967. https://doi.org/10.1016/j.fsi.2012.09.021
CAS Article PubMed Google Scholar
Tomasso JR (1994) Toxicity of nitrogenous wastes to aquatic animals. Rev Fish Sci 2:291–314. https://doi.org/10.1080/10641269409388560
Article Google Scholar
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. https://doi.org/10.1007/s12562-014-0765-3
CAS Article Google Scholar
Wanjugi P, Harwood VJ (2013) The influence of predation and competition on the survival of commensal and pathogenic fecal bacteria in aquatic habitats. Environ. Microbiol 15:517–526. https://doi.org/10.1111/j.1462-2920.2012.02877.x
Article PubMed Google Scholar
Williams TJ, Wilkins D, Long E, Evans F, Demaere MZ, Raftery MJ, Cavicchioli R (2013) The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Mcrobiol 15:1302–1317. https://doi.org/10.1111/1462-2920.12017
CAS Article Google Scholar
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
CAS Article PubMed Google Scholar
Xiong J, Liu Y, Lin X, Zhang H, Zeng J, Hou J, Yang Y, Yao T, Rob K, Chu H (2012) Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environ Mcrobiol 14:2457–2466. https://doi.org/10.1111/j.1462-2920.2012.02799.x
CAS Article Google Scholar
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 Biotechnol 99:6911–6919. https://doi.org/10.1007/s00253-015-6632-z
CAS Article PubMed Google Scholar
Xiong J, Zhu J, Dai W, Dong C, Qiu Q, Li C (2017) Integrating gut microbiota immaturity and disease-discriminatory taxa to diagnose the initiation and severity of shrimp disease. Environ Mcrobiol 19:1490–1501. https://doi.org/10.1111/1462-2920.13701
Article Google Scholar
Xiong J, Zhu J, Zhang D (2014) The application of bacterial indicator phylotypes to predict shrimp health status. Appl Microbiol Biotechnol 98:8291–8299. https://doi.org/10.1007/s00253-014-5941-y
CAS Article PubMed Google Scholar
Xu WJ, Pan LQ (2014) Evaluation of dietary protein level on selected parameters of immune and antioxidant systems, and growth performance of juvenile Litopenaeus vannamei reared in zero-water exchange biofloc-based culture tanks. Aquaculture 426:181–188. https://doi.org/10.1016/j.aquaculture.2014.02.003
CAS Article Google Scholar
Zhang D, Wang X, Xiong J, Zhu J, Wang Y, Zhao Q, Chen H, Guo A, Wu J, Dai H (2014) Bacterioplankton assemblages as biological indicators of shrimp health status. Ecol Indic 38:218–224. https://doi.org/10.1016/j.ecolind.2013.11.002
CAS Article Google Scholar
Zhang H, Sun Z, Liu B, Xuan Y, Jiang M, Pan Y, Zhang Y, Gong Y, Lu X, Yu D (2016) Dynamic changes of microbial communities in Litopenaeus vannamei cultures and the effects of environmental factors. Aquaculture 455:97–108. https://doi.org/10.1016/j.aquaculture.2016.01.011
Article Google Scholar
Zheng Y, Yu M, Liu Y, Su Y, Xu T, Yu M, Zhang XH (2016) Comparison of cultivable bacterial communities associated with Pacific white shrimp (Litopenaeus vannamei) larvae at different health statuses and growth stages. Aquaculture 451:163–169. https://doi.org/10.1016/j.aquaculture.2015.09.020
Article Google Scholar
Zokaeifar H, Babaei N, Che RS, Kamarudin MS, Sijam K, Balcazar JL (2014) Administration of Bacillus subtilis strains in the rearing water enhances the water quality, growth performance, immune response, and resistance against Vibrio harveyi infection in juvenile white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 36:68–74. https://doi.org/10.1016/j.fsi.2013.10.007
CAS Article PubMed Google Scholar

Download references

Acknowledgments

This study was supported by the Key Laboratory of Mariculture (KLM2017005), Ministry Education, Ocean University of China (OUC) and Bio-Form Ecological Environment Corporation of Shandong (20160359). The funders had no role in the study design, data collection, and interpretation and the decision to submit the work for publication.

Author information

Luqing Pan
Present address: Fisheries College, Ocean University of China, Yushan Road 5, Qingdao, 266003, China

Affiliations

The Key Laboratory of Mariculture (Ocean University of China), Ministry of Education, Qingdao, Shandong, China
Fei Huang, Luqing Pan, Mengsi Song, Changcheng Tian & Shuo Gao

Authors

Fei Huang
View author publications
You can also search for this author in PubMed Google Scholar
Luqing Pan
View author publications
You can also search for this author in PubMed Google Scholar
Mengsi Song
View author publications
You can also search for this author in PubMed Google Scholar
Changcheng Tian
View author publications
You can also search for this author in PubMed Google Scholar
Shuo Gao
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luqing Pan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The experiment was permitted by the Institutional Animal Care and Use Committee of the Ocean University of China.

Electronic supplementary material

ESM 1

(PDF 852 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Huang, F., Pan, L., Song, M. et al. Microbiota assemblages of water, sediment, and intestine and their associations with environmental factors and shrimp physiological health. Appl Microbiol Biotechnol 102, 8585–8598 (2018). https://doi.org/10.1007/s00253-018-9229-5

Download citation

Received: 01 January 2018
Revised: 04 July 2018
Accepted: 05 July 2018
Published: 23 July 2018
Issue Date: October 2018
DOI: https://doi.org/10.1007/s00253-018-9229-5

Keywords

Microbial communities
Rearing water
Sediment
Intestine
Shrimp health
Environmental factor