Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective

Abstract Background Pacific Whiteleg shrimp (Litopenaeus vannamei) is an important model for breeding programs to improve global aquaculture productivity. However, the interaction between host genetics and microbiota in enhancing productivity remains poorly understood. We investigated the effect of...

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Main Authors: Fernanda Cornejo-Granados, Luigui Gallardo-Becerra, Sandra Romero-Hidalgo, Alonso A. Lopez-Zavala, Andrés Cota-Huízar, Melany Cervantes-Echeverría, Rogerio R. Sotelo-Mundo, Adrian Ochoa-Leyva
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Animal Microbiome
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Online Access:https://doi.org/10.1186/s42523-025-00414-y
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author Fernanda Cornejo-Granados
Luigui Gallardo-Becerra
Sandra Romero-Hidalgo
Alonso A. Lopez-Zavala
Andrés Cota-Huízar
Melany Cervantes-Echeverría
Rogerio R. Sotelo-Mundo
Adrian Ochoa-Leyva
author_facet Fernanda Cornejo-Granados
Luigui Gallardo-Becerra
Sandra Romero-Hidalgo
Alonso A. Lopez-Zavala
Andrés Cota-Huízar
Melany Cervantes-Echeverría
Rogerio R. Sotelo-Mundo
Adrian Ochoa-Leyva
author_sort Fernanda Cornejo-Granados
collection DOAJ
description Abstract Background Pacific Whiteleg shrimp (Litopenaeus vannamei) is an important model for breeding programs to improve global aquaculture productivity. However, the interaction between host genetics and microbiota in enhancing productivity remains poorly understood. We investigated the effect of two shrimp genetic lines, Fast-Growth (Gen1) and Disease-Resistant (Gen2), on the microbiota of L. vannamei. Results Using genome-wide SNP microarray analysis, we confirmed that Gen1 and Gen2 represented distinct genetic populations. After confirming that the rearing pond did not significantly influence the microbiota composition, we determined that genetic differences explained 15.8% of the microbiota variability, with a stronger selective pressure in the hepatopancreas than in the intestine. Gen1, which exhibited better farm productivity, fostered a microbiota with greater richness, diversity, and resilience than Gen2, along with a higher abundance of beneficial microbes. Further, we demonstrated that a higher abundance of beneficial microbes was associated with healthier shrimp vs. diseased specimens, suggesting that Gen1 could improve shrimp's health and productivity by promoting beneficial microbes. Finally, we determined that the microbiota of both genetic lines was significantly different from their wild-type counterparts, suggesting farm environments and selective breeding programs strongly alter the natural microbiome. Conclusions This study highlights the importance of exploring the hologenome perspective, where integrating host genetics and microbiome composition can enhance breeding programs and farming practices.
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spelling doaj-art-c02abe5a093742f8bbc22f53ea887bb12025-08-20T03:08:43ZengBMCAnimal Microbiome2524-46712025-05-017111710.1186/s42523-025-00414-yHost genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspectiveFernanda Cornejo-Granados0Luigui Gallardo-Becerra1Sandra Romero-Hidalgo2Alonso A. Lopez-Zavala3Andrés Cota-Huízar4Melany Cervantes-Echeverría5Rogerio R. Sotelo-Mundo6Adrian Ochoa-Leyva7Departamento de Microbiología Molecular, Instituto de Biotecnología (IBT), Universidad Nacional Autónoma de México (UNAM)Departamento de Microbiología Molecular, Instituto de Biotecnología (IBT), Universidad Nacional Autónoma de México (UNAM)Departamento de Genómica Computacional, Instituto Nacional de Medicina Genómica, Secretaría de Salud (INMEGEN)Departamento de Ciencias Químico Biológicas, Universidad de Sonora (UNISON)Camarones El Renacimiento SPR de RIDepartamento de Microbiología Molecular, Instituto de Biotecnología (IBT), Universidad Nacional Autónoma de México (UNAM)Laboratorio de Estructura Biomolecular, Centro de Investigación en Alimentación y Desarrollo, A.C. (CIAD)Departamento de Microbiología Molecular, Instituto de Biotecnología (IBT), Universidad Nacional Autónoma de México (UNAM)Abstract Background Pacific Whiteleg shrimp (Litopenaeus vannamei) is an important model for breeding programs to improve global aquaculture productivity. However, the interaction between host genetics and microbiota in enhancing productivity remains poorly understood. We investigated the effect of two shrimp genetic lines, Fast-Growth (Gen1) and Disease-Resistant (Gen2), on the microbiota of L. vannamei. Results Using genome-wide SNP microarray analysis, we confirmed that Gen1 and Gen2 represented distinct genetic populations. After confirming that the rearing pond did not significantly influence the microbiota composition, we determined that genetic differences explained 15.8% of the microbiota variability, with a stronger selective pressure in the hepatopancreas than in the intestine. Gen1, which exhibited better farm productivity, fostered a microbiota with greater richness, diversity, and resilience than Gen2, along with a higher abundance of beneficial microbes. Further, we demonstrated that a higher abundance of beneficial microbes was associated with healthier shrimp vs. diseased specimens, suggesting that Gen1 could improve shrimp's health and productivity by promoting beneficial microbes. Finally, we determined that the microbiota of both genetic lines was significantly different from their wild-type counterparts, suggesting farm environments and selective breeding programs strongly alter the natural microbiome. Conclusions This study highlights the importance of exploring the hologenome perspective, where integrating host genetics and microbiome composition can enhance breeding programs and farming practices.https://doi.org/10.1186/s42523-025-00414-yMicrobiota-host interactionsMicrobiomeMetagenomicsBreedingGenetic line
spellingShingle Fernanda Cornejo-Granados
Luigui Gallardo-Becerra
Sandra Romero-Hidalgo
Alonso A. Lopez-Zavala
Andrés Cota-Huízar
Melany Cervantes-Echeverría
Rogerio R. Sotelo-Mundo
Adrian Ochoa-Leyva
Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
Animal Microbiome
Microbiota-host interactions
Microbiome
Metagenomics
Breeding
Genetic line
title Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
title_full Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
title_fullStr Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
title_full_unstemmed Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
title_short Host genome drives the microbiota enrichment of beneficial microbes in shrimp: exploring the hologenome perspective
title_sort host genome drives the microbiota enrichment of beneficial microbes in shrimp exploring the hologenome perspective
topic Microbiota-host interactions
Microbiome
Metagenomics
Breeding
Genetic line
url https://doi.org/10.1186/s42523-025-00414-y
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