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Cited by 302Aquaculture disease management and microbiotaGut microbiota and healthMicrobial Community Ecology and Physiology

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Microbiome of Pacific Whiteleg shrimp reveals differential bacterial community composition between Wild, Aquacultured and AHPND/EMS outbreak conditions

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Cornejo-Granados, Fernanda, Lopez-Zavala, Alonso A., Gallardo-Becerra, Luigui, Mendoza-Vargas, Alfredo, Sánchez, Filiberto, Vichido, Rodrigo, Brieba, Luis G., Viana, Maria Teresa, Sotelo-Mundo, Rogerio R., Ochoa-Leyva, Adrián·2017·Scientific Reports
DOI 10.1038/s41598-017-11805-wPMC PMC5603525
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Abstract

Crustaceans form the second largest subphylum on Earth, which includes Litopeneaus vannamei (Pacific whiteleg shrimp), one of the most cultured shrimp worldwide. Despite efforts to study the shrimp microbiota, little is known about it from shrimp obtained from the open sea and the role that aquaculture plays in microbiota remodeling. Here, the microbiota from the hepatopancreas and intestine of wild type (wt) and aquacultured whiteleg shrimp and pond sediment from hatcheries were characterized using sequencing of seven hypervariable regions of the 16S rRNA gene. Cultured shrimp with AHPND/EMS disease symptoms were also included. We found that (i) microbiota and their predicted metagenomic functions were different between wt and cultured shrimp; (ii) independent of the shrimp source, the microbiota of the hepatopancreas and intestine was different; (iii) the microbial diversity between the sediment and intestines of cultured shrimp was similar; and (iv) associated to an early development of AHPND/EMS disease, we found changes in the microbiome and the appearance of disease-specific bacteria. Notably, under cultured conditions, we identified bacterial taxa enriched in healthy shrimp, such as Faecalibacterium prausnitzii and Pantoea agglomerans, and communities enriched in diseased shrimp, such as Aeromonas taiwanensis, Simiduia agarivorans and Photobacterium angustum.

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Figure 1 Shrimp sample collection and general microbiota characteristics. (a) Litopenaeus vannamei specimen collection points. Wt shrimp were collected from the Mexican Pacific area 5 km from the state coast (green star), while cultured shrimp were collected from hatchery ponds (orange star) located in the state of Sonora, Mexico. Healthy and AHPND/EMS-diseased shrimp were collected from ponds adjacent to each other. The map was created using the online edition of SmartDraw https://www.smartdraw.com/. (b) Anatomical location of the dissected hepatopancreas and intestine. Taxonomic diversity and abundance of all 24 of the sequenced samples at: (c) phylum; and (d) family levels.
Figure 1 Shrimp sample collection and general microbiota characteristics. (a) Litopenaeus vannamei specimen collection points. Wt shrimp were collected from the Mexican Pacific area 5 km from the state coast (green star), while cultured shrimp were collected from hatchery ponds (orange star) located in the state of Sonora, Mexico. Healthy and AHPND/EMS-diseased shrimp were collected from ponds adjacent to each other. The map was created using the online edition of SmartDraw https://www.smartdraw.com/. (b) Anatomical location of the dissected hepatopancreas and intestine. Taxonomic diversity and abundance of all 24 of the sequenced samples at: (c) phylum; and (d) family levels.CC BY · PubMed Central
Figure 2 Alpha diversity indices. (a) Phylogenetic diversity (PD). (b) Number of observed OTUs. (c) Shannon index. All of the analyzed groups showed significant differences after a Mann-Whitney test with a confidence level of 99% (p ≤ 0.01) in each index. The average value for each group of samples (n = 3) is shown next to each boxplot, and the mean is indicated in red.
Figure 2 Alpha diversity indices. (a) Phylogenetic diversity (PD). (b) Number of observed OTUs. (c) Shannon index. All of the analyzed groups showed significant differences after a Mann-Whitney test with a confidence level of 99% (p ≤ 0.01) in each index. The average value for each group of samples (n = 3) is shown next to each boxplot, and the mean is indicated in red.CC BY · PubMed Central
Figure 3 Beta diversity analysis. Unweighted principal coordinate analysis (PCoA) of UniFrac distances: (a) samples tagged as wt and cultured; and (b) samples tagged by shrimp organ or sediment. Only the first two components are shown. (c) UPGMA tree of unweighted UniFrac distances. Node value represents the jackknife support, using 1,000 replicates.
Figure 3 Beta diversity analysis. Unweighted principal coordinate analysis (PCoA) of UniFrac distances: (a) samples tagged as wt and cultured; and (b) samples tagged by shrimp organ or sediment. Only the first two components are shown. (c) UPGMA tree of unweighted UniFrac distances. Node value represents the jackknife support, using 1,000 replicates.CC BY · PubMed Central
Figure 4 Relative abundance and LEfSe results of enriched microbiota and predicted microbiome functions between wt (n = 3) and cultured intestine (n = 3) samples. (a) Relative abundance of significantly different species. Linear discriminant analysis (LDA) score is shown in parenthesis. (b) LDA of the differentially abundant KEEG pathways. The differences were significant (p < 0.05) among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.
Figure 4 Relative abundance and LEfSe results of enriched microbiota and predicted microbiome functions between wt (n = 3) and cultured intestine (n = 3) samples. (a) Relative abundance of significantly different species. Linear discriminant analysis (LDA) score is shown in parenthesis. (b) LDA of the differentially abundant KEEG pathways. The differences were significant (p < 0.05) among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.CC BY · PubMed Central
Figure 5 Relative abundance and LEfSe results of enriched microbiota and predicted microbiome functions between wt (n = 3) and cultured hepatopancreas (n = 3) samples. (a) Relative abundance of significantly differentially abundant species. Linear discriminant analysis (LDA) score is shown in parenthesis. (b) LDA of the differentially abundant KEEG pathways. The differences were significant (p < 0.05), among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.
Figure 5 Relative abundance and LEfSe results of enriched microbiota and predicted microbiome functions between wt (n = 3) and cultured hepatopancreas (n = 3) samples. (a) Relative abundance of significantly differentially abundant species. Linear discriminant analysis (LDA) score is shown in parenthesis. (b) LDA of the differentially abundant KEEG pathways. The differences were significant (p < 0.05), among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.CC BY · PubMed Central
Figure 6 Relative abundance and LEfSe results of the differentially abundant species between healthy (n = 3) and diseased cultured (n = 3) shrimp. (a) Intestine, (b) hepatopancreas, and (c) sediment samples. LDA score is shown in parenthesis. The differences were significant (p < 0.05) among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.
Figure 6 Relative abundance and LEfSe results of the differentially abundant species between healthy (n = 3) and diseased cultured (n = 3) shrimp. (a) Intestine, (b) hepatopancreas, and (c) sediment samples. LDA score is shown in parenthesis. The differences were significant (p < 0.05) among classes (Kruskal-Wallis test) and subclasses (Wilcoxon’s test). The threshold of the logarithmic LDA score was 2.0.CC BY · PubMed Central

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Metadata

Authors
Cornejo-Granados, F., Lopez-Zavala, A. A., Gallardo-Becerra, L., Mendoza-Vargas, A., Sánchez, F., Vichido, R., Brieba, L. G., Viana, M. T., Sotelo-Mundo, R. R., & Ochoa-Leyva, A.
Affiliations
  • Universidad Nacional Autónoma de México (MX)
  • Secretaria de Salud (MX)
  • Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (MX)
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2017-09-18
Volume
7
Issue
1
Pages
11783-11783
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/s41598-017-11805-w
PMC
PMC5603525
OpenAlex
W2754347595
Cited by
302
References
78
Citations by year
2026: 13 · 2025: 28 · 2024: 39 · 2023: 43 · 2022: 44 · 2021: 45 · 2020: 39 · 2019: 23 · 2018: 26
FWCI
10.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Instituto Nacional de Pesca y Acuacultura
  • Instituto Nacional de Medicina Genómica
  • Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (IA203516)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
Litopenaeus vannamei, aquaculture, wild shrimp, hepatopancreas, intestine, pond sediments, bacterial community composition, 16S rRNA gene, Faecalibacterium prausnitzii, Pantoea agglomerans
MeSH terms
Gastrointestinal Microbiome, Animals, Bacteria, Aquaculture, Penaeidae, Metagenomics

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