Microbiome mediating methane and nitrogen transformations in a subterranean estuary

• Published in: Environmental microbiology 2024-01, Vol.26 (1), p.e16558-n/a
• Main Authors: Euler, Sebastian, Jeffrey, Luke C., Maher, Damien T., Johnston, Scott G., Sugimoto, Ryo, Tait, Douglas R.
• Format: Article
• Language: English
• Subjects: Abundance; Ammonia; Ammonium; Ammonium Compounds; Biogeochemistry; Carbon; Carbon dioxide; Coastal ecosystems; Dissolved organic carbon; Dissolved Organic Matter; Estuaries; Estuarine dynamics; Fluxes; Gases; Greenhouse effect; Greenhouse Gases; Methane; Methanogenic bacteria; Microbial activity; Microbiomes; Microbiota - genetics; Microorganisms; Nitrification; Nitrogen; Nutrients; Pore water; Prokaryotes; Relative abundance; RNA, Ribosomal, 16S - genetics; rRNA 16S; Small mammals; Spatial distribution; Transformations; Zonation
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.16558

Subterranean estuaries (STEs) are important coastal biogeochemical reactors facilitating unique niches for microbial communities. A common approach in determining STE greenhouse gas and nutrient fluxes is to use terrestrial endmembers, not accounting for microbially mediated transformations throughout the STE. As such, the microbial ecology and spatial distribution of specialists that cycle compounds in STEs remain largely underexplored. In this study, we applied 16S rRNA amplicon sequencing with paired biogeochemical characterisations to spatially evaluate microbial communities transforming greenhouse gases and nutrients in an STE. We show that methanogens are most prevalent at the terrestrial end (up to 2.81% relative abundance) concomitant to the highest porewater methane, carbon dioxide and dissolved organic carbon concentrations (0.41 ± 0.02 μM, 273.31 ± 6.05 μM and 0.51 ± 0.02 mM, respectively). Lower ammonium concentrations corresponded with abundant nitrifying and ammonia‐oxidising prokaryotes in the mixing zone (up to 11.65% relative abundance). Methane, ammonium and dissolved organic carbon concentrations all decreased by >50% from the terrestrial to the oceanic end of the 15 m transect. This study highlights the STE's hidden microbiome zonation, as well as the importance of accounting for microbial transformations mitigating nutrient and greenhouse gas fluxes to the coastal ecosystems. Our study reveals distinct microbial and biogeochemical zones in a subterranean estuary that can mediate transformations of the fluxes of greenhouse gases and nutrients. Contrary to common practices, relying solely on terrestrial endmembers to determine greenhouse gas and nutrient discharges to the coastal ocean may lead to overestimation, as our findings suggest that the microbiome in the subterranean estuary contributes to a significant reduction in greenhouse gas and nutrient loads.