Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression

Postlarval shrimp frequently face threats from acute hepatopancreatic necrosis disease (AHPND). Although AHPND affects both postlarval and adult shrimp, abiotic and biotic factors are distinct between life stages, such as rearing water nutrient levels and host life stage-dependent microbiota. The re...

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Main Authors: Zhongjiang Zhou, Jiaqi Lu, Pingping Zhan, Jinbo Xiong
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/13/4/720
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author Zhongjiang Zhou
Jiaqi Lu
Pingping Zhan
Jinbo Xiong
author_facet Zhongjiang Zhou
Jiaqi Lu
Pingping Zhan
Jinbo Xiong
author_sort Zhongjiang Zhou
collection DOAJ
description Postlarval shrimp frequently face threats from acute hepatopancreatic necrosis disease (AHPND). Although AHPND affects both postlarval and adult shrimp, abiotic and biotic factors are distinct between life stages, such as rearing water nutrient levels and host life stage-dependent microbiota. The response of postlarvae-associated microbiota to AHPND, however, remains largely unexplored compared with its effects on juvenile and adult shrimp. To address this knowledge gap, a comparative analysis of postlarvae-associated microbiota and the ecological processes underlying AHPND progression was performed by sequencing the bacterial V3–V4 hypervariable region of the 16S rRNA gene. AHPND infection was validated by high copies of <i>pirAB</i> genes (Toxin 1) in diseased shrimp hepatopancreas. Advanced AHPND significantly altered the structure of the postlarvae-associated microbiota, with significant enrichment of Bacilli and Bdellovibrionia species in healthy larvae compared with matched AHPND-infected cohorts, although gut microbiota recovery was observed at the late disease stage, corresponding with the cessation of postlarval mortality. AHPND infection explained 11.0% (<i>p</i> < 0.001) of the variance in community structures, whereas postlarvae days post hatching also significantly influenced bacterial communities (7.1% variance, <i>p</i> < 0.001). AHPND-infected shrimp exhibited reduced homogeneous selection and increased dispersal limitation and drift governing their microbiota. These changes were primarily driven by specific microbial lineages, including enriched Bin36 Rhodobacteraceae and Bin11 Flavobacteriaceae, and suppressed Bin63 <i>Vibrio</i> and Bin9 <i>Bacillus</i> in AHPND-infected shrimp. After excluding shrimp age effect, 13 AHPND-discriminatory taxa were identified, accurately distinguishing infected shrimp from healthy individuals with 100% precision. Furthermore, AHPND outbreak weakened the network complexity and stability, which was driven by the suppressed keystone taxa that were positively associated with network robustness. Collectively, our findings deepen the understanding of the inextricable interplay between postlarval shrimp health, microbiota dynamics, and survival, as well as the underlying ecological mechanisms over AHPND progression.
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spelling doaj-art-e4be85702e964d319d7aae4ace5934902025-08-20T03:13:48ZengMDPI AGMicroorganisms2076-26072025-03-0113472010.3390/microorganisms13040720Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND ProgressionZhongjiang Zhou0Jiaqi Lu1Pingping Zhan2Jinbo Xiong3State Key Laboratory for the Quality and Safety of Agro-Products, School of Marine Sciences, Ningbo University, Ningbo 315211, ChinaState Key Laboratory for the Quality and Safety of Agro-Products, School of Marine Sciences, Ningbo University, Ningbo 315211, ChinaKey Laboratory of Aquacultural Biotechnology, Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo 315211, ChinaState Key Laboratory for the Quality and Safety of Agro-Products, School of Marine Sciences, Ningbo University, Ningbo 315211, ChinaPostlarval shrimp frequently face threats from acute hepatopancreatic necrosis disease (AHPND). Although AHPND affects both postlarval and adult shrimp, abiotic and biotic factors are distinct between life stages, such as rearing water nutrient levels and host life stage-dependent microbiota. The response of postlarvae-associated microbiota to AHPND, however, remains largely unexplored compared with its effects on juvenile and adult shrimp. To address this knowledge gap, a comparative analysis of postlarvae-associated microbiota and the ecological processes underlying AHPND progression was performed by sequencing the bacterial V3–V4 hypervariable region of the 16S rRNA gene. AHPND infection was validated by high copies of <i>pirAB</i> genes (Toxin 1) in diseased shrimp hepatopancreas. Advanced AHPND significantly altered the structure of the postlarvae-associated microbiota, with significant enrichment of Bacilli and Bdellovibrionia species in healthy larvae compared with matched AHPND-infected cohorts, although gut microbiota recovery was observed at the late disease stage, corresponding with the cessation of postlarval mortality. AHPND infection explained 11.0% (<i>p</i> < 0.001) of the variance in community structures, whereas postlarvae days post hatching also significantly influenced bacterial communities (7.1% variance, <i>p</i> < 0.001). AHPND-infected shrimp exhibited reduced homogeneous selection and increased dispersal limitation and drift governing their microbiota. These changes were primarily driven by specific microbial lineages, including enriched Bin36 Rhodobacteraceae and Bin11 Flavobacteriaceae, and suppressed Bin63 <i>Vibrio</i> and Bin9 <i>Bacillus</i> in AHPND-infected shrimp. After excluding shrimp age effect, 13 AHPND-discriminatory taxa were identified, accurately distinguishing infected shrimp from healthy individuals with 100% precision. Furthermore, AHPND outbreak weakened the network complexity and stability, which was driven by the suppressed keystone taxa that were positively associated with network robustness. Collectively, our findings deepen the understanding of the inextricable interplay between postlarval shrimp health, microbiota dynamics, and survival, as well as the underlying ecological mechanisms over AHPND progression.https://www.mdpi.com/2076-2607/13/4/720postlarval shrimpprogressed AHPNDdriving lineagesnetwork stabilitybiomarkers
spellingShingle Zhongjiang Zhou
Jiaqi Lu
Pingping Zhan
Jinbo Xiong
Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
Microorganisms
postlarval shrimp
progressed AHPND
driving lineages
network stability
biomarkers
title Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
title_full Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
title_fullStr Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
title_full_unstemmed Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
title_short Postlarval Shrimp-Associated Microbiota and Underlying Ecological Processes over AHPND Progression
title_sort postlarval shrimp associated microbiota and underlying ecological processes over ahpnd progression
topic postlarval shrimp
progressed AHPND
driving lineages
network stability
biomarkers
url https://www.mdpi.com/2076-2607/13/4/720
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AT pingpingzhan postlarvalshrimpassociatedmicrobiotaandunderlyingecologicalprocessesoverahpndprogression
AT jinboxiong postlarvalshrimpassociatedmicrobiotaandunderlyingecologicalprocessesoverahpndprogression