Bioturbation and the role of microniches for sulfate reduction in coastal marine sediments

Abstract

The effects of bioturbation in marine sediments are mainly associated with an increase in oxic and oxidized zones through an influx of oxygen-rich water deeper into the sediment and the rapid transport of particles between oxic and anoxic conditions. However, macrofaunal activity also can increase the occurrence of reduced microniches and anaerobic processes, such as sulfate reduction. Our goal was to determine the two-dimensional distribution of microniches associated with burrows of a ghost shrimp (Neotrypaea californiensis) and to determine microbial activities. In laboratory experiments, detailed measurements of sulfate reduction rates (SRR) were measured by injecting, in a 1 cm grid, radiolabelled sulfate directly into a narrow aquarium (40 cm × 30 cm × 3 cm) containing the complex burrow of an actively burrowing shrimp. Light-coloured oxidized burrow walls, along with black reduced microniches, were clearly visible through the aquarium walls. Direct injection of radiotracers allowed for whole-aquarium incubation to obtain two-dimensional documentation of sulfate reduction. Results indicated SRR were up to three orders of magnitude higher (140-790 nmol SO(4) (2-) cm(-3) day(-1) ) in reduced microniches associated with burrows when compared with the surrounding sediment. Additionally, some of the subsurface sulfate-reducing microniches associated with the burrow system appeared to be zones of dinitrogen fixation. Bioturbation may also lead to decreased sulfate reduction in other microniches and the sum of the activity in all microniches might not result in a total increase of sulfate reduction compared with non-bioturbated control sediments.

Denitrification and Nitrogen Fixation Dynamics in the Area Surrounding an Individual Ghost Shrimp (Neotrypaea californiensis) Burrow System

“…Previous studies have shown that bioturbation can greatly increase coupled nitrification-denitrification rates through the extension of the sediment-water interface, an increase in solute transport, and the oxygenation of sediments (28,29,34). Other studies have shown that bioturbation can significantly increase subsurface benthic N 2 fixation rates, linked to sulfate reduction (5,6), showing that N cycling in bioturbated sediments may be more complex than previously thought. Bioturbation and organic carbon availability.…”

“…It has been known that N 2 fixation, the input of N into the system, plays a role in specific benthic environments, primarily within the photic zone (photosynthetic microbial mats, coral reef sediments, and sediments vegetated by sea grasses and marsh plants) (13,14,17,34,35). Only recently was it shown that subsurface sediments in bioturbated areas can represent habitats of significant N 2 fixation by sulfate-reducing bacteria (SRB) (5,6), further demonstrating that our current understanding of N cycling in benthic environments is limited.…”

Benthic Dinitrogen Fixation Traversing the Oxygen Minimum Zone Off Mauritania (NW Africa)

“…In contrary to the inhibiting effect of bioirrigation through the introduction of O 2 , burrowing organisms can also increase microbial activity in sediments by facilitating burial of organic matter (Aller and Aller, 1986;Christensen et al, 2000;Bertics and Ziebis, 2010;Kristensen et al, 2012). In fact, the organic carbon content was found to be one of the most essential environmental factors that control benthic diazotrophs (Hartwig and Stanley, 1978;Jørgensen, 1983;Howarth et al, 1988;Fulweiler et al, 2007;Gier et al, 2016).…”

“…While bioturbation describes the sediment mixing by benthic organisms, bioirrigation encompasses the exchange of seawater with sediment porewater due to the pumping action of burrowdwelling organisms (Meysman et al, 2006;Kristensen et al, 2012). These processes were associated with increased rates of microbial sulfate reduction (Bertics and Ziebis, 2010) and N 2 fixation (Bertics et al, 2012). Both microbial processes are often coupled in organic-rich sediments (Bertics and Ziebis, 2010;Bertics et al, 2013;Gier et al, 2016).…”

“…These processes were associated with increased rates of microbial sulfate reduction (Bertics and Ziebis, 2010) and N 2 fixation (Bertics et al, 2012). Both microbial processes are often coupled in organic-rich sediments (Bertics and Ziebis, 2010;Bertics et al, 2013;Gier et al, 2016). Additionally, many sulfate reducers carry the nifH gene (Zehr and Turner, 2001;Muyzer and Stams, 2008;Fulweiler et al, 2013;Gier et al, 2016) and actively fix N 2 in culture (Riederer-Henderson and Wilson, 1970), indicating that these bacteria may play a role in supplying bioavailable N to the benthic community Sohm et al, 2011;Fulweiler et al, 2013).…”