Quantitative prediction of shrimp disease incidence via the profiles of gut eukaryotic microbiota

Abstract

One common notion is emerging that gut eukaryotes are commensal or beneficial, rather than detrimental. To date, however, surprisingly few studies have been taken to discern the factors that govern the assembly of gut eukaryotes, despite growing interest in the dysbiosis of gut microbiota-disease relationship. Herein, we firstly explored how the gut eukaryotic microbiotas were assembled over shrimp postlarval to adult stages and a disease progression. The gut eukaryotic communities changed markedly as healthy shrimp aged, and converged toward an adult-microbiota configuration. However, the adult-like stability was distorted by disease exacerbation. A null model untangled that the deterministic processes that governed the gut eukaryotic assembly tended to be more important over healthy shrimp development, whereas this trend was inverted as the disease progressed. After ruling out the baseline of gut eukaryotes over shrimp ages, we identified disease-discriminatory taxa (species level afforded the highest accuracy of prediction) that characteristic of shrimp health status. The profiles of these taxa contributed an overall 92.4% accuracy in predicting shrimp health status. Notably, this model can accurately diagnose the onset of shrimp disease. Interspecies interaction analysis depicted how the disease-discriminatory taxa interacted with one another in sustaining shrimp health. Taken together, our findings offer novel insights into the underlying ecological processes that govern the assembly of gut eukaryotes over shrimp postlarval to adult stages and a disease progression. Intriguingly, the established model can quantitatively and accurately predict the incidences of shrimp disease.

Spatiotemporal successions of shrimp gut microbial colonization: high consistency despite distinct species pool

“…By contrast, time series data show that the composition of gut microbiota is relatively stable within healthy humans from teenage to old age, though the generality of this pattern is still under debate (Greenhalgh et al, 2016). However, it has been shown that gut eukaryotic microbiota reaches a relatively stable, adult-like status during shrimp adult stage (Xiong et al, 2018b). Alternatively, due to relative short timescale sampling, we have not captured a stable status of gut bacterial community in aquatic animals.…”

“…Alternatively, due to relative short timescale sampling, we have not captured a stable status of gut bacterial community in aquatic animals. However, it has been shown that gut eukaryotic microbiota reaches a relatively stable, adult-like status during shrimp adult stage (Xiong et al, 2018b). Within this context, long-term works are required to test whether an adult-like gut bacterial community is general across biomes.…”

Response of host–bacterial colonization in shrimp to developmental stage, environment and disease

“…Thus, to improve the host's fitness, the colonization of the gut microbiota is filtered from the rearing species pool as a result of deterministic processes. However, when the gut histology and availability niches change as the host ages, the initial "winners" will be reassembled, thereby resulting in a host stage-specific gut microbiota (Greenhalgh et al, 2016;Stephens et al, 2015;Xiong et al, 2018;Yan et al, 2016). Instead, water quality tends to be deteriorative and eutrophic over shrimp cultivation (Xiong et al, 2014;Yang et al, 2018), which stresses shrimp and increases the virulence of pathogens (Penttinen, Kinnula, Lipponen, Bamford, & Sundberg, 2016).…”

Quantitative PCR Analysis of Gut Disease-Discriminatory Phyla for Determining Shrimp Disease Incidence

“…For this reason, it is mandatory to distinguish the effects of shrimp age from those of disease on the gut microbiota. By distinguishing between age-and disease-discriminatory taxa, a recent study theoretically exemplified that the profiles of gut eukaryotic disease-discriminatory taxa can accurately stratify shrimp health status (20). Similarly, gut bacterial signatures for red-operculum disease are identified at the species level in crucian carp (12).…”

“…A few attempts have shown that disease-discriminatory lineages at the species level contribute a higher accuracy than those at the coarse phylum level in diagnosing caries (19) and shrimp disease (20). However, designing specific primers of bacterial 16S rRNA genes at the species level remains challenging.…”