Role of crab holobionts in benthic N cycling in mangroves with different trophic status

Abstract

Microbial dinitrogen (N2) fixation and intense bioturbation by macrofauna can contribute to reduce nitrogen (N) limitation in mangrove systems. In particular, crabs are important ecosystem engineers that rework sediments, redistribute organic matter, accelerate nutrient cycling and shape microbial communities in mangrove sediments. Hosting functionally diverse microbial communities, crabs form a discrete ecological unit (a holobiont). In this study, we report rates of respiration, inorganic N fluxes, net N2 fixation, denitrification and dissimilatory nitrate reduction to ammonium (DNRA) measured in the fiddler crab Leptuca thayeri and sesarmid crab Armases rubripes holobionts, which are dominant in oligotrophic and eutrophic mangrove systems of southeast Brazil, respectively. We measured lower biomass-specific rates of respiration and ammonium (NH4+) production for the larger L. thayeri compared to A. rubripes, with very different molar ratios of O2 respiration to NH4+ production (152:1 vs. 20:1, respectively). This suggests a size-metabolism relationship, different food quality or different coupling of N excretion and assimilation by the crab holobionts in the 2 systems. Both crab holobionts contributed to net denitrification and DNRA, with faster N cycling in A. rubripes in the eutrophic system. Net N2 fixation was also detected, with nearly 4-fold higher rates in A. rubripes compared to L. thayeri. Overall, our results illustrate active and complex N cycling associated with the 2 dominant crab holobionts and highlight their potential and overlooked role as important conduits of fixed N, which may double N2 fixation rates in the mangrove’s rhizosphere.