Response of host–bacterial colonization in shrimp to developmental stage, environment and disease

Jinbo Xiong; Wenfang Dai; Qiongfen Qiu; Jinyong Zhu; Wen Yang; Chenghua Li

doi:10.1111/mec.14822

journal article Aug 22, 2018

Response of host–bacterial colonization in shrimp to developmental stage, environment and disease

Jinbo Xiong

Wenfang Dai Qiongfen Qiu Jinyong Zhu Wen Yang

Chenghua Li

Molecular Ecology Vol. 27 No. 18 pp. 3686-3699 · Wiley

View at Publisher Save 10.1111/mec.14822

Abstract

AbstractThe host‐associated microbiota is increasingly recognized to facilitate host fitness, but the understanding of the underlying ecological processes that govern the host–bacterial colonization over development and, particularly, under disease remains scarce. Here, we tracked the gut microbiota of shrimp over developmental stages and in response to disease. The stage‐specific gut microbiotas contributed parallel changes to the predicted functions, while shrimp disease decoupled this intimate association. After ruling out the age‐discriminatory taxa, we identified key features indicative of shrimp health status. Structural equation modelling revealed that variations in rearing water led to significant changes in bacterioplankton communities, which subsequently affected the shrimp gut microbiota. However, shrimp gut microbiotas are not directly mirrored by the changes in rearing bacterioplankton communities. A neutral model analysis showed that the stochastic processes that govern gut microbiota tended to become more important as healthy shrimp aged, with 37.5% stochasticity in larvae linearly increasing to 60.4% in adults. However, this defined trend was skewed when disease occurred. This departure was attributed to the uncontrolled growth of two candidate pathogens (over‐represented taxa). The co‐occurrence patterns provided novel clues on how the gut commensals interact with candidate pathogens in sustaining shrimp health. Collectively, these findings offer updated insight into the ecological processes that govern the host–bacterial colonization in shrimp and provide a pathological understanding of polymicrobial infections.

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References

71

[1]

10.1074/jbc.m111.294744

[2]

10.1111/j.1442-9993.2001.01070.pp.x

[3]

AQSIQ. (2007).The specification for marine monitoring of China‐Part 4: seawater analysis (GB 17378.4‐2007). General administration of quality supervision inspection and quarantine (AQSIQ) of the People's Republic of China. (in Chinese).

[4]

10.1038/ismej.2015.142

[5]

Byrne B. M.(2001).Structural Equation Modeling with AMOS. Basic Concepts Applications & Programming Lawrence Erlbaum Associates.

[6]

QIIME allows analysis of high-throughput community sequencing data

J Gregory Caporaso, Justin Kuczynski, Jesse Stombaugh et al.

Nature Methods 10.1038/nmeth.f.303

[7]

10.1016/j.aquaculture.2017.02.033

[8]

10.1007/s00253-018-8891-y

[9]

10.1016/j.fsi.2018.05.040

[10]

10.1016/j.chemosphere.2017.03.034

[11]

10.1016/j.cell.2014.09.043

[12]

10.1186/1471-2105-13-113

[13]

10.1093/nar/gkl244

[14]

10.1890/0012-9615(1997)067[0345:saaist]2.0.co;2

[15]

Search and clustering orders of magnitude faster than BLAST

Robert C. Edgar

Bioinformatics 10.1093/bioinformatics/btq461

[16]

10.1093/bioinformatics/btr381

[17]

Microbial interactions: from networks to models

Karoline Faust, Jeroen Raes

Nature Reviews Microbiology 10.1038/nrmicro2832

[18]

Freter R. "Mechanisms that control bacterial populations in continuous‐flow culture models of mouse large intestinal flora" Infection and Immunity (1983) 10.1128/iai.39.2.676-685.1983

[19]

10.1038/srep18206

[20]

10.1111/1462-2920.13318

[21]

10.1186/s40168-015-0101-x

[22]

10.1111/are.12628

[23]

10.1038/ni.2608

[24]

10.1371/journal.pcbi.1002743

[25]

10.1111/1462-2920.13255

[26]

10.1073/pnas.1214550110

[27]

Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences

Morgan G I Langille, Jesse Zaneveld, J Gregory Caporaso et al.

Nature Biotechnology 10.1038/nbt.2676

[28]

10.1007/s00248-017-0967-1

[29]

10.1111/anu.12098

[30]

10.3389/fmicb.2016.00333

[31]

10.1136/gut.38.3.306

[32]

FLASH: fast length adjustment of short reads to improve genome assemblies

Tanja Magoč, Steven L. Salzberg

Bioinformatics 10.1093/bioinformatics/btr507

[33]

10.1016/j.tim.2015.07.013

[34]

10.1186/1471-2180-9-123

[35]

10.1890/0012-9658(2001)082[0290:fmmtcd]2.0.co;2

[36]

10.1073/pnas.1218525110

[37]

10.1111/1462-2920.12926

[38]

10.1016/j.tim.2016.02.002

[39]

10.1016/j.fsi.2017.07.054

[40]

10.1007/s00248-016-0781-1

[41]

Microbial nutrient niches in the gut

Fátima C. Pereira, David Berry

Environmental Microbiology 10.1111/1462-2920.13659

[42]

10.1111/cmi.12308

[43]

10.1007/978-3-642-30197-1_377

[44]

R Core Team (2015)

[45]

10.1371/journal.pone.0091853

[46]

10.1111/mec.13177

[47]

Ecological theory as a foundation to control pathogenic invasion in aquaculture

Peter De Schryver, Olav Vadstein

The ISME Journal 10.1038/ismej.2014.84

[48]

10.1128/mbio.00974-15

[49]

Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks

Paul Shannon, Andrew Markiel, Owen Ozier et al.

Genome Research 10.1101/gr.1239303

[50]

Quantifying the roles of immigration and chance in shaping prokaryote community structure

William T. Sloan, Mary Lunn, Stephen Woodcock et al.

Environmental Microbiology 10.1111/j.1462-2920.2005.00956.x

Showing 50 of 71 references

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References

Details

Published: Aug 22, 2018
Vol/Issue: 27(18)
Pages: 3686-3699
License: View

Authors

J

Jinbo Xiong

School of Marine Sciences Ningbo University Ningbo China; Collaborative Innovation Center for Zhejiang Marine High‐Efficiency and Healthy Aquaculture Ningbo University Ningbo China

W

Wenfang Dai

School of Marine Sciences Ningbo University Ningbo China; Collaborative Innovation Center for Zhejiang Marine High‐Efficiency and Healthy Aquaculture Ningbo University Ningbo China

Q

Qiongfen Qiu

School of Marine Sciences Ningbo University Ningbo China

J

Jinyong Zhu

School of Marine Sciences Ningbo University Ningbo China

W

Wen Yang

School of Marine Sciences Ningbo University Ningbo China

C

Chenghua Li

School of Marine Sciences Ningbo University Ningbo China; Collaborative Innovation Center for Zhejiang Marine High‐Efficiency and Healthy Aquaculture Ningbo University Ningbo China

Funding

Ningbo University

Zhejiang Province Public Welfare Technology Application Research Project Award: 2016C32063

Cite This Article

Jinbo Xiong, Wenfang Dai, Qiongfen Qiu, et al. (2018). Response of host–bacterial colonization in shrimp to developmental stage, environment and disease. Molecular Ecology, 27(18), 3686-3699. https://doi.org/10.1111/mec.14822

Response of host–bacterial colonization in shrimp to developmental stage, environment and disease

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