Isopod holobionts as promising models for lignocellulose degradation

Abstract

Background Isopods have colonized all environments, partly thanks to their ability to decompose the organic matter. Their enzymatic repertoire, as well as the one of their associated microbiota, has contributed to their colonization success. Together, these holobionts have evolved several interesting life history traits to degrade the plant cell walls, mainly composed of lignocellulose. It has been shown that terrestrial isopods achieve lignocellulose degradation thanks to numerous and diverse CAZymes provided by both the host and its microbiota. Nevertheless, the strategies for lignocellulose degradation seem more diversified in isopods, in particular in aquatic species which are the least studied. Isopods could be an interesting source of valuable enzymes for biotechnological industries of biomass conversion. Results To provide new features on the lignocellulose degradation in isopod holobionts, shotgun sequencing of 36 metagenomes of digestive and non-digestive tissues was performed from several populations of four aquatic and terrestrial isopod species. Combined to the 15 metagenomes of an additional species from our previous study, as well as the host transcriptomes, this large dataset allowed us to identify the CAZymes in both the host and the associated microbial communities. Analyses revealed the dominance of Bacteroidetes and Proteobacteria in the five species, covering 36% and 56% of the total bacterial community, respectively. The identification of CAZymes and new enzymatic systems for lignocellulose degradation, such as PULs, cellulosomes and LPMOs, highlights the richness of the strategies used by the isopods and their associated microbiota. Conclusions Altogether, our results show that the isopod holobionts are promising models to study lignocellulose degradation. These models can provide new enzymes and relevant lignocellulose-degrading bacteria strains for the biotechnological industries of biomass conversion.

The gut microbiota structure of the terrestrial isopod Porcellionides pruinosus (Isopoda: Oniscidea)

“…On the other hand, the screening of the bacterial community involved in the breakdown of lignocellulose revealed the presence of four phyla within P. pruinosus, five phyla in A. vulgare, four phyla in Porcellio dilatatus dilatatus and Porcellio dilatatus petiti respectively and three phyla within the freshwater isopod Asellus aquaticus (Bredon et al 2020). The same study showed that Proteobacteria and Bacteroidetes phyla dominate the microbiota of the five studied species especially P. pruinosus where they encode the most part of lignocellulose degrading CAZymes.…”

“…In accordance, it has been argued that the host origin is the most important factor shaping the microbiota composition in Oniscidea (Dittmer et al 2016;Delhoumi et al 2018). Indeed, the microbiome reacts more rapidly than its host to environmental variability which aids it to evolve and conquer new niches (Bredon et al 2019(Bredon et al , 2020. Moreover, several studies showed that environmental bacteria are involved in Oniscidea performances like reproductive success, growth rate, survival and fertility (Zimmer 2002b;Horváthová et al 2015;Delhoumi et al 2019b) given their high nutritive value (Zimmer & Topp 1998).…”

“…Furthermore, we found that the digestive tissues of P. pruinosus harbor cellulolytic bacteria involved in the breakdown of cellulose and potentially in the degradation of terrestrial leaf litter mainly composed of lignocelluloses. The fact that the microbiota associated with the digestive tissues of P. pruinosus includes cellulolytic bacteria producing enzymes involved in the degradation of cellulose makes this species useful in industrial processing of lignocellulose and then biofuel production from biomasses as suggested within plant feeding animals like terrestrial isopods (Bredon et al 2020) and lepidoptera (Dantur et al 2015).…”

“…Among Crustacea, Oniscidea are the most successful colonizers of terrestrial habitats. In contrast to several species of marine isopods which don't show microbiota in their digestive tract (Ray & Julian 1952;Besser et al 2018), all the studied terrestrial species showed diverse and rich microbial communities in their digestive tract (Zimmer & Topp 1998;Kostanjšek et al 2002;Zimmer 2002aZimmer , 2004Dittmer et al 2016;Horváthová et al 2016;Bredon et al 2020). A comparative study of the bacterial community associated with the hepatopancreas showed a clear difference between freshwater, semi-terrestrial and terrestrial isopods suggesting that the symbionts acquisition may occur in response to nutritional habits (Wang et al 2007).…”

“…Recent studies showed that terrestrial isopods depend on numerous Carbohydrate Active EnZymes (CAZymes) affiliated to several families to degrade lignocellulose mainly composed by cellulose, lignin and hemicellulose. These enzymes were provided by the host and especially by its associated microbiota (Bredon et al 2018(Bredon et al , 2020.…”