Individual level microbial communities in the digestive system of the freshwater isopod Asellus aquaticus: Complex, robust and prospective

Abstract

The freshwater isopod Asellus aquaticus is an important decomposer of leaf detritus, and its diverse gut microbiome has been depicted as key contributors in lignocellulose degradation as of terrestrial isopods. However, it is not clear whether the individual-level microbiome profiles in the isopod digestive system across different habitats match the implied robust digestion function of the microbiome. Here, we described the bacterial diversity and abundance in the digestive system (hindgut and caeca) of multiple A. aquaticus individuals from two contrasting freshwater habitats. Individuals from a lake and a stream harboured distinct microbiomes, indicating a strong link between the host-associated microbiome and microbes inhabiting the environments. While faeces likely reflected the variations in environmental microbial communities included in the diet, the microbial communities also substantially differed in the hindgut and caeca. Microbes closely related to lignocellulose degradation are found consistently more enriched in the hindgut in each individual. Caeca often associated with taxa implicated in endosymbiotic/parasitic roles (Mycoplasmatales and Rickettsiales), highlighting a complex host-parasite-microbiome interaction. The results highlight the lability of the A. aquaticus microbiome supporting the different functions of the two digestive organs, which may confer particular advantages in freshwater environments characterized by seasonally fluctuating and spatially disparate resource availability.

FIGURE 1

Digestive system of the Asellus aquaticus (Source: adapted from Bronn et al., 1859).Ingested food is mechanically processed in the foregut (oesophagus and stomach). The majority of food processing takes place in the hindgut, and the caeca are responsible for both digestion and absorption. These tube‐like glands secrete digestive fluids to the stomach and process liquids, as well as fine particles from the hindgut.

FIGURE 2

(A) ZOTU distribution and the corresponding abundance in lake and stream individuals. (B) ZOTU distribution and the corresponding abundance in caeca, hindguts, and faeces samples. Within the bracket shows the percentage of the overall abundance and the corresponding abundance. (C) PCoA based on unweighted UniFrac distance matrix showing differences in bacterial community composition between different habitats in different sample types. (D) PCoA based on weighted UniFrac distance matrix showing differences in bacterial community composition among samples from different individuals. Each dot represents a sample, and the number label shows which individual the sample is from. C, caeca; F, faeces; H, hindgut

FIGURE 3

Composition of bacterial communities (relative abundance) in caeca and hindguts. The order of taxa in the legend follows the order of taxa in the community bar (from top to bottom). The 20 most abundant bacterial orders are specified in the legend. Samples are clustered based on unweighted UniFrac distance matrix. C, caeca; F, faeces; H, hindgut

FIGURE 4

Normalized counts of differentially enriched bacterial orders in hindgut and caeca and the corresponding log2FoldChange (hindgut vs. caeca). Only bacterial orders with adjusted p value <0.05 and estimated base mean > 30 are considered as differentially enriched taxa. Unidentified taxa at order level are marked with asterisk. C, caeca; H, hindgut