Mangrove forests are among the most productive and diverse ecosystems on the planet, despite limited nitrogen (N) availability. Under such conditions, animal-microbe associations (holobionts) are often key to ecosystem functioning. Here, we investigated the role of fiddler crabs and their carapaceassociated microbial biofilm as hotspots of microbial N transformations and sources of N within the mangrove ecosystem. 16S rRNA gene and metagenomic sequencing provided evidence of a microbial biofilm dominated by Cyanobacteria, Alphaproteobacteria, Actinobacteria, and Bacteroidota with a community encoding both aerobic and anaerobic pathways of the N cycle. Dinitrogen (N 2) fixation was among the most commonly predicted process. Net N fluxes between the biofilm-covered crabs and the water and microbial N transformation rates in suspended biofilm slurries portray these holobionts as a net N 2 sink, with N 2 fixation exceeding N losses, and as a significant source of ammonium and dissolved organic N to the surrounding environment. N stable isotope natural abundances of fiddler crab carapace-associated biofilms were within the range expected for fixed N, further suggesting active microbial N 2 fixation. These results extend our knowledge on the diversity of invertebratemicrobe associations, and provide a clear example of how animal microbiota can mediate a plethora of essential biogeochemical processes in mangrove ecosystems. Among coastal ecosystems, mangrove forests are of great importance as they account for three quarters of the tropical coastline and provide different ecosystem services 1,2. Mangrove ecosystems generally act as a net sink of carbon, although they release organic matter to the sea in the form of dissolved refractory macromolecules, leaves, branches and other debris 3,4. In pristine environments, mangroves are among the most productive ecosystems on the planet, despite growing in tropical waters that are often nutrient depleted 5. The refractory nature of the organic matter produced and retained in mangroves can slow the recycling of nutrients, particularly of nitrogen (N) 3,6. Nitrogen limitation in such systems may be overcome by microbial dinitrogen (N 2) fixation when combined with high rates of bioturbation by macrofauna 7,8. Bioturbation by macrofauna affect N availability and multiple N-related microbial processes through sediment reworking, burrow construction and bioirrigation, feeding and excretion 9. Macrofauna mix old and fresh organic matter, extend oxic-anoxic sediment interfaces, increase the availability of energy-yielding electron acceptors and increase N turnover via direct excretion 10,11. Thus, macrofauna may alleviate N limitation by priming the remineralization of refractory N, reducing plants-microbe competition 12,13. Such activity ultimately promotes N-recycling, plant assimilation and high N retention, as well as favours it loss by stimulating coupled nitrification and denitrification 14. Mangrove sediments are highly bioturbated by decapods such as crabs 15. Crab populations ...