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

Abstract

Bioturbation is a key process in coastal sediments, influencing microbially driven cycling of nutrients as well as the physical characteristics of the sediment. However, little is known about the distribution, diversity and function of the microbial communities that inhabit the burrows of infaunal macroorganisms. In this study, terminal-restriction fragment length polymorphism analysis was used to investigate variation in the structure of bacterial communities in sediment bioturbated by the burrowing shrimp Upogebia deltaura or Callianassa subterranea. Analyses of 229 sediment samples revealed significant differences between bacterial communities inhabiting shrimp burrows and those inhabiting ambient surface and subsurface sediments. Bacterial communities in burrows from both shrimp species were more similar to those in surface-ambient than subsurface-ambient sediment (R ¼ 0.258, Po0.001). The presence of shrimp was also associated with changes in bacterial community structure in surrounding surface sediment, when compared with sediments uninhabited by shrimp. Bacterial community structure varied with burrow depth, and also between individual burrows, suggesting that the shrimp's burrow construction, irrigation and maintenance behaviour affect the distribution of bacteria within shrimp burrows. Subsequent sequence analysis of bacterial 16S rRNA genes from surface sediments revealed differences in the relative abundance of bacterial taxa between shrimp-inhabited and uninhabited sediments; shrimp-inhabited sediment contained a higher proportion of proteobacterial sequences, including in particular a twofold increase in Gammaproteobacteria. Chao1 and ACE diversity estimates showed that taxon richness within surface bacterial communities in shrimp-inhabited sediment was at least threefold higher than that in uninhabited sediment. This study shows that bioturbation can result in significant structural and compositional changes in sediment bacterial communities, increasing bacterial diversity in surface sediments and resulting in distinct bacterial communities even at depth within the burrow. In an area of high macrofaunal abundance, this could lead to alterations in the microbial transformations of important nutrients at the sediment-water interface.

Impact of ocean acidification on benthic and water column ammonia oxidation

“…Therefore, observed changes in nitrate and ammonia efflux during previous work may reflect differences in other N-cycling processes; dissimilatory nitrate reduction and denitrification; or a reduction in nitrification associated with the activity of macro fauna, which were adversely affected by low pH. Both microbial diversity [Laverock et al, 2010] and nitrification activity are enhanced in the burrow walls of bioturbating fauna [Henriksen et al, 1983;Welsh and Castadelli, 2004]. A decrease in nitrification may thus have occurred as a result of the deleterious effect of OA on macro-fauna during our previous work.…”

Hydraulic activities by ghost shrimp Neotrypaea californiensis induce oxic−anoxic oscillations in sediments

“…Infaunal activities perturb the stratified distribution of metabolites, and, due to the inherent differences in chemical constituents of the overlying water and porewater, bioirrigation creates a distinct functional environment with unique geochemical properties (Aller 1994) and highly heterogeneous distributions of microbial assemblages (Papaspyrou et al 2005, Bertics & Ziebis 2009, Laverock et al 2010. The mosaic of spatially and temporally complex and dynamic geochemical conditions is expected to be a challenging environment for obligate aerobic and anaerobic bacteria, with the relative duration of oxic and anoxic periods being a crucial determinant of microbial activity (Aller 1994, CravoLaureau et al 2011.…”

Characterization of specificity of bacterial community structure within the burrow environment of the marine polychaete Hediste (Nereis) diversicolor

“…However, only a few studies have compared the bacterial community structure of the burrow wall with surface and/or surrounding sediments. They were based on phospholipid fatty acid (PLFA) (Dobbs and Guckert, 1988;Steward et al, 1996;Marinelli et al, 2002) or terminal restriction fragment length polymorphism (T-RFLP) (Laverock et al, 2010) analyses, nucleic acid analyses such as 5S rRNA (Lucas et al, 2003) and 16S rRNA gene fingerprinting or cloning (Matsui et al, 2004;Papaspyrou et al, 2005Papaspyrou et al, , 2006Laverock et al, 2010). Those studies pointed out that the crustacean or annelid burrow walls presented specific microbial communities.…”