Laboratory- and field-based investigation on macrofaunal control of microbial community structure and activity in intertidal sediment

Benthic macrofauna occupy most of the oxygenated seafloor, where they have a strong influence on microbial activity and are major regulators of carbon and other elemental cycles. To explore the yet-elusive relationships between faunal sediment alteration (bioturbation), microbial community structure, and microbial activity, we conducted aquarium incubations of Abarenicola pacifica and Nereis vexillosa in a seawater flow system and field manipulation experiments in a sandy intertidal zone. Microsensor and geochemical profiling show strong impacts of both worms on the pore-water concentrations of electron acceptors (O₂, NO₃^-, and SO₄^-) and metabolites (NH₄⁺, HS^-, and Fe₂⁺), and suggest the distinctly different advective and diffusive type of bioirrigations generated by A. pacifica and N. vexillosa, respectively, in sediment. Comprehensive analyses on microbial community structure and activity using amplicon sequencing and quantitative-(Reverse Transcription)-PCR of 16S rRNA and functional genes suggest that the metabolically active microbial community structure in intertidal sandy sediments is highly resilient to macrofaunal disturbance. This resilience likely stems from metabolic versatility that enables dominant microorganisms to switch between (micro)aerobic and anaerobic lifestyles under the fluctuating redox conditions in these environments. Significant changes of microbial community structure were only locally observed in the fecal pellet and feeding funnel of A. pacifica and mucus of N. vexillosa, likely due to the distinct organic matter composition and/or higher exposure time to oxygen in these microenvironments. Results from the field-based manipulation experiments further suggest that, in addition to macrofaunal bioturbation, conditions of temperature, tidal movement, and supply of photosynthetic organic matter also play important roles in controlling microbial activity and community structure in intertidal sediment.