Species-specific gill’s microbiome of eight crab species with different breathing adaptations

Abstract

Transitions to physically different environments, such as the water-to-land transition, proved to be the main drivers of relevant evolutionary events. Brachyuran crabs evolved remarkable morphological, behavioral, and physiological adaptations to terrestrial life. Terrestrial species evolved new respiratory structures devoted to replace or support the gills, a multifunctional organ devoted to gas exchanges, ion-regulation and nitrogen excretion. It was hypothesized that microorganisms associated with respiratory apparatus could have facilitated the processes of osmoregulation, respiration, and elimination of metabolites along this evolutionary transition. To test if crab species with different breathing adaptations may host similar microbial communities on their gills, we performed a comparative targeted-metagenomic analysis, selecting two marine and six terrestrial crabs belonging to different families and characterised by different breathing adaptations. We analysed anterior and posterior gills separately according to their different and specific roles. Regardless of their terrestrial or marine adaptations, microbial assemblages were strongly species-specific indicating a non-random association between the host and its microbiome. Significant differences were found in only two terrestrial species when considering posterior vs. anterior gills, without any association with species-specific respiratory adaptations. Our results suggest that all the selected species are strongly adapted to the ecological niche and specific micro-habitat they colonise.

Mangrovimonas cancribranchiae sp. nov., a novel bacterial species associated with the gills of the fiddler crab Cranuca inversa (Brachyura, Ocypodidae) from Red Sea mangroves

“…In particular, the gill-associated microbiomes of Cranuca inversa () have been proposed to help the animal in the disposal of ammonia (the primary nitrogenous waste of crabs) during periods of exposure to air and to protect it from other potentially toxic compounds, such as hydrogen sulphide and carbon monoxide [12]. This relationship supports the concept of a true symbiosis that could have contributed (and still does) to the adaptation of these crab species to intertidal environments and, to a broader extent, to the terrestrialization of these animals [11, 12, 14, 15].…”

“…To cope with the challenges posed by such a lifestyle, they have evolved physiological [7], morphological [8] and behavioural [9] adaptations, including structural modifications of their gills, which are key organs in the evolutionary adaptation of crabs. Recently, microbial communities associated with the gills of mangrove fiddler crabs have been described [10][11][12][13][14], garnering attention for their potential symbiotic and coevolutionary implications. In particular, the gill-associated microbiomes of Cranuca inversa (Fig.…”

“…To cope with the challenges posed by such a lifestyle, they have evolved physiological [7], morphological [8] and behavioural [9] adaptations, including structural modifications of their gills, which are key organs in the evolutionary adaptation of crabs. Recently, microbial communities associated with the gills of mangrove fiddler crabs have been described [10–14], garnering attention for their potential symbiotic and coevolutionary implications. In particular, the gill-associated microbiomes of Cranuca inversa () have been proposed to help the animal in the disposal of ammonia (the primary nitrogenous waste of crabs) during periods of exposure to air and to protect it from other potentially toxic compounds, such as hydrogen sulphide and carbon monoxide [12].…”