Influences of Infaunal Burrows on the Community Structure and Activity of Ammonia-Oxidizing Bacteria in Intertidal Sediments

Abstract

Influences of infaunal burrows constructed by the polychaete (Tylorrhynchus heterochaetus) on O 2 concentrations and community structures and abundances of ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB) in intertidal sediments were analyzed by the combined use of a 16S rRNA gene-based molecular approach and microelectrodes. The microelectrode measurements performed in an experimental system developed in an aquarium showed direct evidence of O 2 transport down to a depth of 350 mm of the sediment through a burrow. The 16S rRNA gene-cloning analysis revealed that the betaproteobacterial AOB communities in the sediment surface and the burrow walls were dominated by Nitrosomonas sp. strain Nm143-like sequences, and most of the clones in Nitrospira-like NOB clone libraries of the sediment surface and the burrow walls were related to the Nitrospira marina lineage. Furthermore, we investigated vertical distributions of AOB and NOB in the infaunal burrow walls and the bulk sediments by real-time quantitative PCR (Q-PCR) assay. The AOB and Nitrospira-like NOB-specific 16S rRNA gene copy numbers in the burrow walls were comparable with those in the sediment surfaces. These numbers in the burrow wall at a depth of 50 to 55 mm from the surface were, however, higher than those in the bulk sediment at the same depth. The microelectrode measurements showed higher NH 4 ؉ consumption activity at the burrow wall than those at the surrounding sediment. This result was consistent with the results of microcosm experiments showing that the consumption rates of NH 4 ؉ and total inorganic nitrogen increased with increasing infaunal density in the sediment. These results clearly demonstrated that the infaunal burrows stimulated O 2 transport into the sediment in which otherwise reducing conditions prevailed, resulting in development of high NH 4 ؉ consumption capacity. Consequently, the infaunal burrow became an important site for NH 4 ؉ consumption in the intertidal sediment.Benthic infaunal activities, such as burrow formation, burrow irrigation, defecation, and excretion of soluble and insoluble metabolites, increase the surface area across which solutes can diffuse into or out of the sediments and the substrate availability for inhabiting microorganisms (5,13,17,24,25,32,34). These burrows also provide a more stable physical environment compared to bulk sediment. Therefore, the sediment surrounding the infaunal burrows (i.e., burrow walls) could have markedly higher levels of microbial biomass, diversity, and activity compared with the bulk sediment. Previous studies have revealed that benthic infaunal activities resulted in changes in biogeochemical characteristics and microbial community structures in sediments (20,22,31). Although many studies demonstrated that the presence of benthic infauna strongly affects the microbial ecology of estuarine sediments, surprisingly little attention has been paid to bioturbation effects on nitrification. In estuarine systems with high inputs of nitrogenous compounds, sedim...

Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments

“…It is possible that such changes may in addition influence the function and activity of bacterial communities within the burrow. For example, the presence of U. deltaura in sediments has been shown to lead to significant increases in total denitrification rates (Howe et al, 2004), while numbers of ammonia-oxidising bacteria were greater at certain depths within a polychaete burrow than in the surrounding sediment (Satoh et al, 2007).…”

Modelling Marine Sediment Biogeochemistry: Current Knowledge Gaps, Challenges, and Some Methodological Advice for Advancement

“…Without understanding this variability, benthic systems may exhibit apparently paradoxical behaviour. For instance, nitrification in deep nominally anoxic sediment layers (Satoh et al, 2007), occurring as a consequence of burrowing fauna pumping oxygenated waters into the deeper sediment, locally modifying redox conditions (Wenzhöfer and Glud, 2004;Volkenborn et al, 2010). Biogeochemical models mostly consider bio-irrigation (biological enhancement of solute transfer) as a factor enhancing the diffusion coefficient (Blackford, 1997;Reed et al, 2011), resulting in a thicker oxic layer near the sediment surface.…”

“…It has been shown that burrowing activity of benthic macrofauna can lead to as much as 400% increase in denitrification rates (Gilbert et al, 1998;Webb and Eyre, 2004), mostly due to the high rates of nitrification occurring within the burrows (Howe et al, 2004). Burrows thus offer an ideal environment for diverse microbial communities to work very closely and efficiently: indeed, genetic analysis has shown that in-burrow bacterial communities are more similar to the surface sediment community than the ambient sediment community at similar depth (Satoh et al, 2007;Laverock et al, 2010). Conversely, anaerobic microniches may be formed in surface aerobic sediments when the consumption rate due to the mineralisation of POM by bacteria is higher than the oxygen diffusion into the particle.…”

Life history of the copepod Hemicyclops spinulosus (Poecilostomatoida, Clausidiidae) associated with crab burrows with notes on male polymorphism and precopulatory mate guarding

“…It is possible that H. spinulosus possesses hemoglobin, which may be highly advantageous in the low-oxygen environment in the mud-flat sediments (e.g. Satoh et al 2007), but this awaits confirmation.…”