Background:

Sesarmid crabs dominate mangrove habitat as the major primary consumers, which facilitates the trophic link and nutrient recycling in the ecosystem. Therefore, the adaptations and mechanisms of sesarmid crabs to herbivory is not only crucial to terrestrialization and its evolutionary success, but also to the healthy functioning of mangrove forest ecosystems. Although endogenous cellulases expressions were reported in crab species, it remains unknown if the endogenous enzymes alone can complete the whole lignocellulolytic pathway, or they also depend on the contribution from their intestinal microbiome. We attempt to investigate the role of gut symbiotic microbes of mangrove-feeding sesarmid crabs in plant digestion using a comparative metagenomic approach.

Results:

Metagenomics analyses on 43 crab gut samples from 23 species of mangrove crabs revealed a wide coverage of 127 CAZy families and nine KOs targeting lignocellulose and their derivatives in all species analyzed, including predominantly carnivorous species, suggesting the crab species gut microbiome have lignocellulolytic capacity regardless of dietary preference. Microbial cellulase, hemicellulase and pectinase genes in herbivorous and detritivorous crabs were differentially more abundant when compared to omnivorous and carnivorous crabs, indicating the importance of gut symbionts in lignocellulose degradation in mangrove crabs and the enrichment of lignocellulolytic microbes in response to diet with higher lignocellulose content. The herbivorous and detritivorous crabs showed highly similar CAZyme composition compared to dissimilarities observed in taxonomic profiles observed in both groups, suggesting a stronger selection force to gut microbiota by its functional capacity than by taxonomy. The gut microbiota in herbivorous sesarmid crabs were also enriched with nitrogen reduction and fixation genes, implying possible roles of the gut microbiota in supplementing nitrogen that is deficient in plant diet.

Conclusions:

Endosymbiotic cellulolytic microbes play an important role in lignocellulose degradation in most crab species but their abundance is strongly correlated with dietary preference, and they are highly enriched in herbivorous sesarmids, thus enhancing their capacity for digestion of mangrove leaves. Dietary preference is a stronger driver in determining the microbial CAZyme composition and taxonomic profile in mangrove crab microbiome, resulting in functional redundancy of endosymbiotic microbes. Our results showed that crabs implement a mixed mode of digestion utilizing both endogenous and microbial enzymes in lignocellulose degradation, as observed in most of the more advanced herbivorous invertebrate species.