Burrowing deeper into benthic nitrogen cycling: the impact of bioturbation on nitrogen fixation coupled to sulfate reduction

Biological dinitrogen (N-2) fixation is the primary input of fixed nitrogen (N) into the marine biosphere, making it an essential process contributing to the biological functions of all organisms. Because biologically available N often limits marine productivity, microbial processes leading to its loss and gain (e. g. denitrification and N-2 fixation, respectively) play an important role in global biogeochemical cycles. Bioturbation is known to influence benthic N cycling, most often reported as enhancement of denitrification and a subsequent loss of N-2 from the system. N-2 fixation has rarely been addressed in bioturbation studies. Instead, sedimentary N-2 fixation typically has been considered important in relatively rare, localized habitats such as rhizosphere and phototrophic microbial mat environments. However, the potential for N-2 fixation in marine sediments may be more widespread. We show here that nitrogenase activity can be very high (up to 5 nmol C2H4 cm(-3) h(-1)) in coastal sediments bioturbated by the ghost shrimp Neotrypaea californiensis and at depths below 5 cm. Integrated subsurface N-2-fixation rates were greater than those previously found for un-vegetated estuarine sediments and were comparable to rates from photosynthetic microbial mats and rhizospheres. Inhibition experiments and genetic analysis showed that this activity was mainly linked to sulfate reduction. Sulfate-reducing bacteria (SRB) are widespread and abundant in marine sediments, with many possessing the genetic capacity to fix N-2. Our results show that N-2 fixation by SRB in bioturbated sediments may be an important process leading to new N input into marine sediments. Given the ubiquity of bioturbation and of SRB in marine sediments, this overlooked benthic N-2 fixation may play an important role in marine N and carbon (C) cycles.