The inverted microbial loop stimulates mineralisation of sedimentary organic detritus

Abstract

Respiration is a key process in the organic carbon cycle of marine sediments, the understanding of which is key to future management decisions which aim to maximise sediment carbon storage. The microbial community is typically considered the dominant actor in overall sedimentary respiration, but knowledge is lacking about interactions with other components, particularly the macrofauna. The “inverted microbial loop” hypothesis suggests that macrofaunal activity stimulates the microbial respiration of organic carbon through the mixing of fresh organic carbon to depth, and subsequent priming (i.e. activation of refractory detritus by co-respiration with fresh detritus). We conducted experimental incubations to partition respiration amongst the microbial and macrofaunal components of the community and investigate interactions between them. We prepared sediment cores with native benthic communities, macrofauna only and microbial communities only. We added 13C labelled fresh organic matter to these cores and measured respiration over 7 d, quantifying both O2 consumption (reflecting remineralisation of all sedimentary organic C) and production of 13C dissolved inorganic C (DIC, reflecting remineralisation of labile organic C). Consumption of O2, which reflected remineralisation of ambient as well as added fresh organic C, showed greater rates when macrofaunal and microbial communities were present together than the sum of their separate rates. This provides direct experimental evidence that the inverted microbial loop mechanism stimulates mineralisation of less reactive, ambient organic C. Macrofaunal and microbial communities showed approximately equal contributions to the total community respiration, suggesting that faunal respiration should be more routinely included in carbon degradation modelling. The fate of the added fresh organic C in different treatments suggested competition for this resource between macrofauna and microbes, and some functional redundancy amongst different components of the benthic community. The enhanced understanding of sediment respiration generated by this study has implications for management of shelf seafloors to balance carbon storage with other human uses.