The Impacts of Invertebrate Activities on Sediment Microbial Community and Functional Ecology

Abstract

Sediment nitrogen cycling is a network of microbially-mediated biogeochemical processes that can regulate ecosystem functioning. As invertebrate activity is known to affect sediment microbial communities, producing accurate models of benthic nitrogen cycling requires an understanding of the interactions between invertebrates, microbial communities and biogeochemical processes. Few invertebrate activity assessments have included detailed microbial analysis and there is a general bias towards a narrow range of invertebrate activities that relate to particle reworking and burrow ventilation. The aim of this study was to use contemporary molecular techniques to expand our understanding of invertebrate-microbe interactions in relation to three invertebrate activities. First, despite previous research on burrow ventilation, burrow morphology effects on microbial communities remain poorly characterised. This study identified clear differences in the abundance and activity of ammonia-oxidising microbial groups between open and closed burrow morphologies, but only at mid-mixing sediment depths. Vertical depth variation should therefore be considered in future invertebrate trait assessments. Second, this study confirmed previously unverified claims that nitrogen-rich invertebrate mucopolysaccharide secretions stimulate nitrification and denitrification processes. These effects can also be altered by mucus concentration and redox oscillations, and could therefore differ between invertebrate taxa with varying mucus lining thicknesses or ventilation periodicities. Finally, using high-throughput sequencing, this study examined two additional understudied invertebrate traits: internal gut transit and external surface transport. These findings demonstrated that the gut tracts of the marine worm Hediste diversicolor contain a unique transitory microbial community that could support a distinct assemblage of ammonia-oxidising archaea, and identified a unique external microbial community. Both of these traits could play a role in mediating microbial distribution and transport within sediment environments. Overall, this study identified several understudied invertebrate activities and characterised their effects on sediment microbial communities and specific nitrogen cycling functional groups. The burrow morphology research also highlighted the importance of re-examining invertebrate activities with contemporary molecular techniques to gain further insight into invertebrate-microbe interaction mechanisms. Incorporating these additional traits and more robust microbial analyses into sediment ecosystem models could help to build the ecological complexity needed to better predict future changes to sediment nitrogen budgets and other ecologically critical biogeochemical processes.

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ORCID for Martin Solan: orcid.org/0000-0001-9924-5574

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