Comparative analysis of gut microbiome of mangrove brachyuran crabs revealed patterns of phylosymbiosis and codiversification

The acquisition of microbial symbionts enables animals to rapidly adapt to
and exploit novel ecological niches, thus significantly enhancing the
evolutionary fitness and success of their hosts. However, the dynamics of
host-microbe interactions and their evolutionary implications remain
largely underexplored in marine invertebrates. Crabs of the family
Sesarmidae (Crustacea: Brachyura) are dominate inhabitants of mangrove
forests and considered as keystone species there. Their rapid
diversification, particularly after adopting a plant-feeding lifestyle, is
believed to have been facilitated by symbiotic gut microbes, enabling
successful colonization of intertidal and terrestrial environments. To
investigate the patterns and mechanisms shaping the microbial communities
and the role of microbes in the evolution of Sesarmidae, we characterized
and compared the gut microbiome compositions across 43 crab species from
Sesarmidae and other mangrove-associated families using 16S metabarcoding.
We found that the gut microbiome assemblages in crabs are primarily
determined by host identity, with a secondary influence from environmental
factors such as microhabitat and sampling location, and to a lesser extent
influenced by biological factors such as sex and gut region. While
patterns of phylosymbiosis (i.e. when microbial community relationships
recapitulate the phylogeny of their hosts) were consistently observed in
all beta-diversity metrics analyzed, the strength of phylosymbiosis varied
across crab families. This suggests that the bacterial assemblages in each
family were differentially shaped by different degrees of host filtering
and/or other evolutionary processes. Notably, Sesarmidae displayed signals
of cophylogeny with its core gut bacterial genera, which likely play
crucial functional roles in their hosts by providing lignocellulolytic
enzymes, essential amino acids and fatty acids supplementation. Our
results support the hypothesis of microbial contribution to herbivory and
terrestrialization in mangrove crabs, highlighting the tight association
and codiversification of the crab holobiont. Benefit-Sharing Statement
This work provides access to new 16S microbiome data sets obtained from
the digestive tract of 43 species of crabs, many of which are ecologically
important species in intertidal and terrestrial environments. Our analyses
have provided a comprehensive protocol in the study of core microbiome,
phylosymbiosis and codiversification in non-model organisms, which could
provide a methodological reference to fuel microbial research on other
understudied non-model organisms.