Vertically stratified methane, nitrogen and sulphur cycling and coupling mechanisms in mangrove sediment microbiomes

Mangrove ecosystems are considered as hot spots of biogeochemical cycling, yet the diversity, function and coupling mechanism of microbially driven biogeochemical cycling along the sediment depth of mangrove wetlands remain elusive. Here we investigated the vertical profile of methane (CH₄), nitrogen (N) and sulphur (S) cycling genes/pathways and their potential coupling mechanisms using metagenome sequencing approaches.

Our results showed that the metabolic pathways involved in CH₄, N and S cycling were mainly shaped by pH and acid volatile sulphide (AVS) along a sediment depth, and AVS was a critical electron donor impacting mangrove sediment S oxidation and denitrification. Gene families involved in S oxidation and denitrification significantly (P < 0.05) decreased along the sediment depth and could be coupled by S-driven denitrifiers, such as Burkholderiaceae and Sulfurifustis in the surface sediment (0-15 cm). Interestingly, all S-driven denitrifier metagenome-assembled genomes (MAGs) appeared to be incomplete denitrifiers with nitrate/nitrite/nitric oxide reductases (Nar/Nir/Nor) but without nitrous oxide reductase (Nos), suggesting such sulphide-utilizing groups might be an important contributor to N₂O production in the surface mangrove sediment. Gene families involved in methanogenesis and S reduction significantly (P < 0.05) increased along the sediment depth. Based on both network and MAG analyses, sulphate-reducing bacteria (SRB) might develop syntrophic relationships with anaerobic CH₄ oxidizers (ANMEs) by direct electron transfer or zero-valent sulphur, which would pull forward the co-existence of methanogens and SRB in the middle and deep layer sediments.

In addition to offering a perspective on the vertical distribution of microbially driven CH₄, N and S cycling genes/pathways, this study emphasizes the important role of S-driven denitrifiers on N₂O emissions and various possible coupling mechanisms of ANMEs and SRB along the mangrove sediment depth. The exploration of potential coupling mechanisms provides novel insights into future synthetic microbial community construction and analysis. This study also has important implications for predicting ecosystem functions within the context of environmental and global change. Video Abstract.