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

Abstract

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.

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

“…Under these premises, discriminatory populations relating to life stage in shrimp gut are differed from these in rearing bacterioplankton communities. This pattern could be affected by, or attributed to, the effect of host selection, which supports the notion that host gut microbial community is not a simple mirror of their rearing environmental counterparts (Burns et al, 2016;Li et al, 2017;Zhang et al, 2018;Xiong et al, 2018a). Instead, shrimp selects specific bacteria (independent of their abundances in environmental pool) at a given life stage (Walke et al, 2014).…”

“…Intriguingly, a high stratification accuracy (95.5%) of shrimp life stages was achieved by using profiles of the top four gut age-discriminatory genera as independent variables (Figs. This pattern could be affected by, or attributed to, the effect of host selection, which supports the notion that host gut microbial community is not a simple mirror of their rearing environmental counterparts (Burns et al, 2016;Li et al, 2017;Zhang et al, 2018;Xiong et al, 2018a). By contrast, the four genera in water did not contribute comparable stratification accuracy for bacterioplankton communities.…”

“…However, from a host perspective, it is pivotal to select a beneficial microbiota, and thereby exclude foreign pathogenic strains (Mcfall-Ngai et al, 2013). Indeed, microbiota in the host gut is frequently detected to be significantly less diverse than that in the surrounding environmental samples, i.e., sediment and water (Hou et al, 2018;Xiong et al, 2018a), suggesting that factors within the host are further regulating the bacterial communities. Indeed, microbiota in the host gut is frequently detected to be significantly less diverse than that in the surrounding environmental samples, i.e., sediment and water (Hou et al, 2018;Xiong et al, 2018a), suggesting that factors within the host are further regulating the bacterial communities.…”

“…By this logic, there are distinct gut bacterial communities in cohabitating fishes with varied tropic levels (Yan et al, 2016), and even in cohabitating larvae of four different species within the family Cyprinidae (Li et al, 2012). Indeed, microbiota in the host gut is frequently detected to be significantly less diverse than that in the surrounding environmental samples, i.e., sediment and water (Hou et al, 2018;Xiong et al, 2018a), suggesting that factors within the host are further regulating the bacterial communities. On the bacterial side, niche theory predicts that competition with other commensals in the gut barriers against external invaders, that is, colonization resistance (Hecht et al, 2016;Xiong et al, 2018a).…”

“…Indeed, microbiota in the host gut is frequently detected to be significantly less diverse than that in the surrounding environmental samples, i.e., sediment and water (Hou et al, 2018;Xiong et al, 2018a), suggesting that factors within the host are further regulating the bacterial communities. On the bacterial side, niche theory predicts that competition with other commensals in the gut barriers against external invaders, that is, colonization resistance (Hecht et al, 2016;Xiong et al, 2018a). With regard to gut microbiota of aquatic animals, commensals could disperse from its rearing water, for example, via passive dispersal and host selection (Burns et al, 2016;Yan et al, 2016;Xiong et al, 2017b).…”