Summary Mangroves are forest ecosystems located at the interface between land and sea where sediments presented a variety of contrasted environmental conditions (i.e. oxic/anoxic, non‐sulfidic/sulfidic, organic matter content) providing an ideal ecosystem to study microbial communities with niche differentiation and distinct community structures. In this work, prokaryotic and fungal compositions were investigated during both wet and dry seasons in New Caledonian mangrove sediments, from the surface to deeper horizons under the two most common tree species in this region (Avicennia marina and Rhizophora stylosa), using high‐throughput sequencing. Our results showed that Bacteria and Archaea communities were mainly shaped by sediment depth while the fungal community was almost evenly distributed according to sediment depth, vegetation cover and season. A detailed analysis of prokaryotic and fungal phyla showed a dominance of Ascomycota over Basidiomycota whatever the compartment, while there was a clear shift in prokaryotic composition. Some prokaryotic phyla were enriched in surface layers such as Proteobacteria, Euryarchaeota while others were mostly associated with deeper layers as Chloroflexi, Bathyarchaeota, Aminicenantes. Our results highlight the importance of considering fungal and prokaryotic counterparts for a better understanding of the microbial succession involved in plant organic matter decomposition in tropical coastal sediments.

The functional diversity of the New Caledonian mangrove sediments was examined, observing the distribution of fungal dye-decolorizing peroxidases (DyPs), together with the complete biochemical characterization of the main DyP. Using a functional metabarcoding approach, the diversity of expressed genes encoding fungal DyPs was investigated in surface and deeper sediments, collected beneath either Avicennia marina or Rhizophora stylosa trees, during either the wet or the dry seasons. The highest DyP diversity was observed in surface sediments beneath the R. stylosa area during the wet season, and one particular operational functional unit (OFU1) was detected as the most abundant DyP isoform. This OFU was found in all sediment samples, representing 51–100% of the total DyP-encoding sequences in 70% of the samples. The complete cDNA sequence corresponding to this abundant DyP (OFU 1) was retrieved by gene capture, cloned, and heterologously expressed in Pichia pastoris. The recombinant enzyme, called DyP1, was purified and characterized, leading to the description of its physical–chemical properties, its ability to oxidize diverse phenolic substrates, and its potential to decolorize textile dyes; DyP1 was more active at low pH, though moderately stable over a wide pH range. The enzyme was very stable at temperatures up to 50 °C, retaining 60% activity after 180 min incubation. Its ability to decolorize industrial dyes was also tested on Reactive Blue 19, Acid Black, Disperse Blue 79, and Reactive Black 5. The effect of hydrogen peroxide and sea salt on DyP1 activity was studied and compared to what is reported for previously characterized enzymes from terrestrial and marine-derived fungi.