Increasing evidence has emerged a tight link among the gut microbiota, host age and health status. This osculating interplay impedes the definition of gut microbiome features associated with host health from that in developmental stages. Consequently, gut microbiota-based prediction of health status is promising yet not well established. Here we firstly tracked shrimp gut microbiota (N = 118) over an entire cycle of culture; shrimp either stayed healthy or progressively transitioned into severe disease. The results showed that the gut microbiota were significantly distinct over shrimp developmental stages and disease progression. Null model and phylogenetic-based mean nearest taxon distance (MNTD) analyses indicated that deterministic processes that governed gut community became less important as the shrimp aged and disease progressed. The predicted gut microbiota age (using the profiles of age-discriminatory bacterial species as independent variables) fitted well (r = 0.996; P < 0.001) with the age of healthy subjects, while this defined trend was disrupted by disease. Microbiota-for-age Z-scores (MAZ, here defined as immaturity) were relative stable among healthy shrimp, but sharply decreased when disease emerged. By distinguishing between age- and disease- discriminatory taxa, we developed a model, bacterial indicators of shrimp health status, to diagnose disease from healthy subjects with 91.5% accuracy. Notably, the relative abundances of the bacterial indicators were indicative for shrimp disease severity. These findings, in aggregate, add our understanding on the gut community assembly patterns over shrimp developmental stages and disease progression. In addition, shrimp disease initiation and severity can be accurately diagnosed using gut microbiota immaturity and bacterial indicators.

Intestinal bacterial communities play a pivotal role in promoting host health; therefore, the disruption of intestinal bacterial homeostasis could result in disease. However, the effect of the occurrences of disease on intestinal bacterial community assembly remains unclear. To address this gap, we compared the multifaceted ecological differences in maintaining intestinal bacterial community assembly between healthy and diseased shrimps. The neutral model analysis shows that the relative importance of neutral processes decreases when disease occurs. This pattern is further corroborated by the ecosphere null model, revealing that the bacterial community assembly of diseased samples is dominated by stochastic processes. In addition, the occurrence of shrimp disease reduces the complexity and cooperative activities of species-to-species interactions. The keystone taxa affiliated with Alphaproteobacteria and Actinobacteria in healthy shrimp gut shift to Gammaproteobacteria species in diseased shrimp. Changes in intestinal bacterial communities significantly alter biological functions in shrimp. Within a given metabolic pathway, the pattern of enrichment or decrease between healthy and deceased shrimp is correlated with its functional effects. We propose that stressed shrimp are more prone to invasion by alien strains (evidenced by more stochastic assembly and higher migration rate in diseased shrimp), which, in turn, disrupts the cooperative activity among resident species. These findings greatly aid our understanding of the underlying mechanisms that govern shrimp intestinal community assembly between health statuses.

The 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.

High-density aquaculture has led to increasing occurrences of diseases in shrimp. Thus, it is imperative to establish effective and quantitative strategies for preventing and predicting these diseases. Water quality indices and investigations of specific pathogen abundance provide only a qualitative evaluation of the risk of shrimp disease and can be inaccurate. To address these shortcomings, we introduced intestinal indicative assemblages as independent variables with which to quantitatively predict incidences of shrimp disease. Given the ignorance regarding the niches differences in the shrimp intestine throughout its developmental stages, the use of probiotics in aquaculture has had limited success. Therefore, we propose the exploration of effective probiotic bacteria from shrimp intestinal flora and the establishment of therapeutic strategies dependent on shrimp age. Following ecological selection principles, we hypothesize that the larval stage provides the best opportunity to establish a desired gut microbiota through preemptive colonization of the treated rearing water with known probiotics. To employ this strategy, however, substantial barriers must be overcome.

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Increasing evidence of tight links among the gut microbiota, obesity, and host health has emerged, but knowledge of the ecological processes that shape the variation in microbial assemblages across growth rates remains elusive. Moreover, inadequately control for differences in factors that profoundly affect the gut microbial community, hampers evaluation of the gut microbiota roles in regulating growth rates. To address this gap, we evaluated the composition and ecological processes of the gut bacterial community in cohabitating retarded, overgrown, and normal shrimps from identically managed ponds. Gut bacterial community structures were distinct (P = 0.0006) among the shrimp categories. Using a structural equation modeling (SEM), we found that changes in the gut bacterial community were positively related to digestive activities, which subsequently affected shrimp growth rate. This association was further supported by intensified interspecies interaction and enriched lineages with high nutrient intake efficiencies in overgrown shrimps. However, the less phylogenetic clustering of gut microbiota in overgrown and retarded subjects may offer empty niches for pathogens invasion, as evidenced by higher abundances of predicted functional pathways involved in disease infection. Given no differences in biotic and abiotic factors among the cohabitating shrimps, we speculated that the distinct gut community assembly could be attributed to random colonization in larval shrimp (e.g., priority effects) and that an altered microbiota could be a causative factor in overgrowth or retardation in shrimp. To our knowledge, this is the first study to provide an integrated overview of the direct roles of gut microbiota in shaping shrimp growth rate and the underlying ecological mechanisms.

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Increasing evidence has revealed a close interplay between the gut bacterial communities and host growth performance. However, until recently, studies generally ignored the contribution of eukaryotes, endobiotic organisms. To fill this gap, we used Illumina sequencing technology on eukaryotic 18S rRNA gene to compare the structures of gut eukaryotic communities among cohabitating retarded, overgrown, and normal shrimp obtained from identically managed ponds. Results showed that a significant difference between gut eukaryotic communities differed significantly between water and intestine and among three shrimp categories. Structural equation modeling revealed that changes in the gut eukaryotic community were positively related to digestive enzyme activities, which in turn influenced shrimp growth performance (λ = 0.97, P < 0.001). Overgrown shrimp exhibited a more complex and cooperative gut eukaryotic interspecies interaction than retarded and normal shrimp, which may facilitate their nutrient acquisition efficiency. Notably, the distribution of dominant eukaryotic genera and shifts in keystone species were closely concordant with shrimp growth performance. In summary, this study provides an integrated overview on direct roles of gut eukaryotic communities in shrimp growth performance instead of well-studied bacterial assembly.