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.

Tolerance to environmental pollution in the freshwater crustacean Asellus aquaticus: A role for the microbiome

“…Hence, we hypothesised that the microbiome (i.e., transient or already established community) could help to buffer the isopod host against the negative effects of MPs through the ability to degrade and metabolise the organic pollutants (Claus et al, 2016). In general, the bacterial community of both (donor) adults and juveniles was dominated by bacterial phyla Proteobacteria , Actinomycetota , Bacillota, Bacteroidota, and Tenericutes , that also dominate in other terrestrial and aquatic isopods (Bredon et al, 2020; Dittmer et al, 2016; Horvathova et al, 2016; Horváthová et al, 2019; Lafuente et al, 2023; Liao et al, 2023; Oliveira et al, 2021). The most abundant taxa were members of Dermabacteraceae ( Actinomycetota), Micrococcaceae (Actinomycetota), Flavobacteriaceae (Bacteroidota), Xanthomonadaceae (Proteobacteria), Pseudomonaceae (Proteobacteria), which have been shown to contribute to the lignocellulose degradation in diverse isopods including A. aquaticus (Bredon et al, 2020; Delhoumi et al, 2020).…”

“…Freshwater isopods derive the majority of gut microbes from the environment (i.e., transient community) as microbial members present in the water or associated with leaves are typically found also in their digestive tract (Liao et al, 2023). The environmental microbes in our study were exposed to the MPs, providing the potential to adjust to the pollution.…”

“…The species tolerates a wide range of environmental pollutants including polycyclic aromatic hydrocarbons, endocrine‐disrupting compounds, radionuclide contaminants or nanoparticles (Maltby, 1991; O'Callaghan et al, 2019), and is able to accumulate heavy metals (Goodyear & McNeill, 1999). The gut microbiome is typically diverse and differs both at the individual and at the population level (Lafuente et al, 2023; Liao et al, 2023), with a considerable fraction of the gut microbes derived from environmental sources (Liao et al, 2023). We aimed to assess whether the bacterial component of the microbiome of A. aquaticus plays a role in coping with environmental pollution by so‐called micropollutants (MPs), including pesticides, pharmaceuticals, consumer products, and industrial chemicals, using faecal microbial transplants and fitness quantification of naïve juveniles.…”

Effects of anthropogenic stress on hosts and their microbiomes: Treated wastewater alters performance and gut microbiome of a key detritivore (Asellus aquaticus)

“…Importantly, A. aquaticus (as many other isopod species) has a highly diverse gut microbiota in its hepatopancreas (i.e. midgut gland, thereafter called “midgut”) and hindgut (Bredon et al, 2020 ), with important eco‐evolutionary roles (Bouchon et al, 2016 ; Liao et al, 2023 ). Hepatopancreatic symbionts, for example, are thought to enable isopods to digest leaf litter as well as to aid the host in detoxifying chemical compounds (Bouchon et al, 2016 ; Bredon et al, 2020 ; Zimmer & Bartholmé, 2003 ).…”