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A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota

The shrimp or prawn is the most valuable traded marine product in the world market today and its microbiota plays an essential role in its development, physiology, and health. The technological advances and dropping costs of high-throughput sequencing have increased the number of studies characteriz...

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Autores principales: Cornejo-Granados, Fernanda, Gallardo-Becerra, Luigui, Leonardo-Reza, Miriam, Ochoa-Romo, Juan Pablo, Ochoa-Leyva, Adrian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6089209/
https://www.ncbi.nlm.nih.gov/pubmed/30128187
http://dx.doi.org/10.7717/peerj.5382
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author Cornejo-Granados, Fernanda
Gallardo-Becerra, Luigui
Leonardo-Reza, Miriam
Ochoa-Romo, Juan Pablo
Ochoa-Leyva, Adrian
author_facet Cornejo-Granados, Fernanda
Gallardo-Becerra, Luigui
Leonardo-Reza, Miriam
Ochoa-Romo, Juan Pablo
Ochoa-Leyva, Adrian
author_sort Cornejo-Granados, Fernanda
collection PubMed
description The shrimp or prawn is the most valuable traded marine product in the world market today and its microbiota plays an essential role in its development, physiology, and health. The technological advances and dropping costs of high-throughput sequencing have increased the number of studies characterizing the shrimp microbiota. However, the application of different experimental and bioinformatics protocols makes it difficult to compare different studies to reach general conclusions about shrimp microbiota. To meet this necessity, we report the first meta-analysis of the microbiota from freshwater and marine shrimps using all publically available sequences of the 16S ribosomal gene (16S rRNA gene). We obtained data for 199 samples, in which 63.3% were from marine (Alvinocaris longirostris, Litopenaeus vannamei and Penaeus monodon), and 36.7% were from freshwater (Macrobrachium asperulum, Macrobrachium nipponense, Macrobranchium rosenbergii, Neocaridina denticulata) shrimps. Technical variations among studies, such as selected primers, hypervariable region, and sequencing platform showed a significant impact on the microbiota structure. Additionally, the ANOSIM and PERMANOVA analyses revealed that the most important biological factor in structuring the shrimp microbiota was the marine and freshwater environment (ANOSIM R = 0.54, P = 0.001; PERMANOVA pseudo-F = 21.8, P = 0.001), where freshwater showed higher bacterial diversity than marine shrimps. Then, for marine shrimps, the most relevant biological factors impacting the microbiota composition were lifestyle (ANOSIM R = 0.341, P = 0.001; PERMANOVA pseudo-F = 8.50, P = 0.0001), organ (ANOSIM R = 0.279, P = 0.001; PERMANOVA pseudo-F = 6.68, P = 0.001) and developmental stage (ANOSIM R = 0.240, P = 0.001; PERMANOVA pseudo-F = 5.05, P = 0.001). According to the lifestyle, organ, developmental stage, diet, and health status, the highest diversity were for wild-type, intestine, adult, wild-type diet, and healthy samples, respectively. Additionally, we used PICRUSt to predict the potential functions of the microbiota, and we found that the organ had more differentially enriched functions (93), followed by developmental stage (12) and lifestyle (9). Our analysis demonstrated that despite the impact of technical and bioinformatics factors, the biological factors were also statistically significant in shaping the microbiota. These results show that cross-study comparisons are a valuable resource for the improvement of the shrimp microbiota and microbiome fields. Thus, it is important that future studies make public their sequencing data, allowing other researchers to reach more powerful conclusions about the microbiota in this non-model organism. To our knowledge, this is the first meta-analysis that aims to define the shrimp microbiota.
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spelling pubmed-60892092018-08-20 A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota Cornejo-Granados, Fernanda Gallardo-Becerra, Luigui Leonardo-Reza, Miriam Ochoa-Romo, Juan Pablo Ochoa-Leyva, Adrian PeerJ Aquaculture, Fisheries and Fish Science The shrimp or prawn is the most valuable traded marine product in the world market today and its microbiota plays an essential role in its development, physiology, and health. The technological advances and dropping costs of high-throughput sequencing have increased the number of studies characterizing the shrimp microbiota. However, the application of different experimental and bioinformatics protocols makes it difficult to compare different studies to reach general conclusions about shrimp microbiota. To meet this necessity, we report the first meta-analysis of the microbiota from freshwater and marine shrimps using all publically available sequences of the 16S ribosomal gene (16S rRNA gene). We obtained data for 199 samples, in which 63.3% were from marine (Alvinocaris longirostris, Litopenaeus vannamei and Penaeus monodon), and 36.7% were from freshwater (Macrobrachium asperulum, Macrobrachium nipponense, Macrobranchium rosenbergii, Neocaridina denticulata) shrimps. Technical variations among studies, such as selected primers, hypervariable region, and sequencing platform showed a significant impact on the microbiota structure. Additionally, the ANOSIM and PERMANOVA analyses revealed that the most important biological factor in structuring the shrimp microbiota was the marine and freshwater environment (ANOSIM R = 0.54, P = 0.001; PERMANOVA pseudo-F = 21.8, P = 0.001), where freshwater showed higher bacterial diversity than marine shrimps. Then, for marine shrimps, the most relevant biological factors impacting the microbiota composition were lifestyle (ANOSIM R = 0.341, P = 0.001; PERMANOVA pseudo-F = 8.50, P = 0.0001), organ (ANOSIM R = 0.279, P = 0.001; PERMANOVA pseudo-F = 6.68, P = 0.001) and developmental stage (ANOSIM R = 0.240, P = 0.001; PERMANOVA pseudo-F = 5.05, P = 0.001). According to the lifestyle, organ, developmental stage, diet, and health status, the highest diversity were for wild-type, intestine, adult, wild-type diet, and healthy samples, respectively. Additionally, we used PICRUSt to predict the potential functions of the microbiota, and we found that the organ had more differentially enriched functions (93), followed by developmental stage (12) and lifestyle (9). Our analysis demonstrated that despite the impact of technical and bioinformatics factors, the biological factors were also statistically significant in shaping the microbiota. These results show that cross-study comparisons are a valuable resource for the improvement of the shrimp microbiota and microbiome fields. Thus, it is important that future studies make public their sequencing data, allowing other researchers to reach more powerful conclusions about the microbiota in this non-model organism. To our knowledge, this is the first meta-analysis that aims to define the shrimp microbiota. PeerJ Inc. 2018-08-10 /pmc/articles/PMC6089209/ /pubmed/30128187 http://dx.doi.org/10.7717/peerj.5382 Text en ©2018 Cornejo-Granados et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Aquaculture, Fisheries and Fish Science
Cornejo-Granados, Fernanda
Gallardo-Becerra, Luigui
Leonardo-Reza, Miriam
Ochoa-Romo, Juan Pablo
Ochoa-Leyva, Adrian
A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title_full A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title_fullStr A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title_full_unstemmed A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title_short A meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
title_sort meta-analysis reveals the environmental and host factors shaping the structure and function of the shrimp microbiota
topic Aquaculture, Fisheries and Fish Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6089209/
https://www.ncbi.nlm.nih.gov/pubmed/30128187
http://dx.doi.org/10.7717/peerj.5382
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