Methanogens limited to lower rhizosphere and to an atypical salt marsh niche along a pristine intertidal mangrove continuum

Abstract

Mangroves are valuable ecosystems that facilitate primary production, carbon sequestration, and regulation of greenhouse gas (GHG) cycles in coastal sediments, with microorganisms playing key roles. Specialized bacteria and archaea compete for energy and resources in mangrove sediments to inhabit optimal ecological niches and can produce or consume methane (CH4)—a potent GHG—in the process. CH4 cycling in mangroves has gained growing attention, yet uncertainties regarding functional and spatial distributions of microorganisms remain. Here, we demonstrate that in a pristine mangrove forest, CH4 concentrations and methanogen communities are concentrated within lower or below rhizosphere depths. We also reveal atypical niches for methanogens in the upper tidal salt marsh zone where vegetation is sparse and highest methanogens abundances were detected at deepest depths (4715 reads g−1) despite relatively high redox potentials (> 250 mV). Pore water CH4 concentrations were highest at the deepest depth within the mangrove forest (max. 3.40 ± 0.21 μM) and coincided with the highest sediment CH4 fluxes (276.4 ± 54.2 μmol m−2d−1) and methanotroph abundances at the surface (1309 reads g−1). Sediment CH4 oxidation fractions between the deepest (60 cm) and shallowest (5 cm) depths were estimated between 18.8% and 64.9%. Positive correlation between crab burrows and CH4 fluxes suggests that CH4 from deeper sediment and salt marsh niches can be transported via conduits to the atmosphere. The spatial data from this study highlights the importance of investigating CH4 dynamics across estuarine ecosystem gradients to better understand the complex roles of vital coastal vegetation zones in the face of a changing climate.