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Even though sediment macrofauna are widespread in the global seafloor, the influence of these fauna on microbial communities that drive sediment biogeochemical cycles remains poorly understood. According to recent field investigations, macrofaunal activities control bacterial and archaeal community structure in surface sediments, but the inferred mechanisms have not been experimentally verified. Here we use laboratory microcosms to investigate how activities of two major polychaete guilds, the lugworms, represented byAbarenicola pacifica, and the clamworms, represented byNereis vexillosa, influence microbial communities in coastal sediments.A. pacificatreatments show >tenfold increases in microbial cell-specific consumption rates of oxygen and nitrate, largely due to the strong ventilation activity ofA. pacifica. While ventilation resulted in clearly elevated percentages of nitrifying archaea (Nitrosopumilusspp.) in surface sediments, it only minorly affected bacterial community composition. By comparison, reworking – mainly by deposit-feeding ofA. pacifica– had a more pronounced impact on microorganismal communities, significantly driving down abundances of Bacteria and Archaea. Within the Bacteria, lineages that have been linked to the degradation of microalgal biomass (e.g., Flavobacteriaceae and Rhodobacteraceae), were especially affected, consistent with the previously reported selective feeding ofA. pacificaon microalgal detritus. In contrast,N. vexillosa, which is not a deposit feeder, did not significantly influence microbial abundances or microbial community structure. This species also only had a relatively minor impact on rates of oxygen and nitrogen cycling, presumably because porewater exchanges during burrow ventilation by this species were mainly restricted to sediments immediately surrounding the burrows. Collectively our analyses demonstrate that macrofauna with distinct bioturbation modes differ greatly in their impacts on microbial community structure and microbial metabolism in marine sediments. 

Abstract Intertidal sands are global hotspots of terrestrial and marine carbon cycling with strong hydrodynamic forcing by waves and tides and high macrofaunal activity. Yet, the relative importance of hydrodynamics and macrofauna in controlling these ecosystems remains unclear. Here, we compare geochemical gradients and bacterial, archaeal, and eukaryotic gene sequences in intertidal sands dominated by subsurface deposit-feeding worms (Abarenicola pacifica) to adjacent worm-free areas. We show that hydrodynamic forcing controls organismal assemblages in surface sediments, while in deeper layers selective feeding by worms on fine, algae-rich particles strongly decreases the abundance and richness of all three domains. In these deeper layers, bacterial and eukaryotic network connectivity decreases, while percentages of clades involved in degradation of refractory organic matter, oxidative nitrogen, and sulfur cycling increase. Our findings reveal macrofaunal activity as the key driver of biological community structure and functioning, that in turn influence carbon cycling in intertidal sands below the mainly physically controlled surface layer.