A bioturbator, a holobiont, and a vector: The multifaceted role of Chironomus plumosus in shaping N-cycling

Tube-dwelling chironomid larvae are among the few taxa that can withstand and thrive in the organic-rich sediments typical of eutrophic freshwater ecosystems. They can have multiple effects on microbial nitrogen (N) cycling in burrow environments, but such effects cease when chironomid larvae undergo metamorphosis into flying adults and leave the sediment. Here we investigated the ecological role of Chironomus plumosus by exploring the effect of its different life stages (as larva and adult midge) on microbial N transformations in a shallow freshwater lagoon by means of combined biogeochemical and molecular approaches. Results suggest that sediment bioturbation by chironomid larvae produce contrasting effects on nitrate (NO3-)-reduction processes. Denitrification was the dominant pathway of NO3- reduction (>90%), primarily fuelled by NO3- from bottom water. In addition to pumping NO3--rich bottom water within the burrows, chironomid larvae host microbiota capable of NO3- reduction. However, the contribution of larval microbiota is lower than that of microbes inhabiting the burrow walls. Interestingly, dinitrogen fixation co-occurred with NO3- reduction processes, indicating versatility of the larvae's microbial community. Assuming all larvae (averaging 1,800 ind./m(2)) leave the sediment following metamorphosis into flying adults, we estimated a displacement of 47,787 mu mol of organic N/m(2) from the sediment to the atmosphere during adult emergence. This amount of particulate organic N is similar to the entire N removal stimulated by larvae denitrification over a period of 20 days. Finally, the detection of N-cycling marker genes in flying adults suggests that these insects retain N-cycling microbes during metamorphosis and migration to the aerial and terrestrial ecosystems. This study provides evidence that chironomids have a multifaceted role in shaping the N cycle of aquatic ecosystems.

Automated summary

The study found that tube-dwelling chironomid larvae play a multifaceted role in shaping the nitrogen cycle in aquatic ecosystems, with significant impacts on denitrification processes. The larvae contribute to nitrate reduction primarily through denitrification, with additional effects from dinitrogen fixation, highlighting the versatility of their microbial community. Detection of nitrogen-cycling marker genes in flying adults suggests that chironomids retain nitrogen-cycling microbes during metamorphosis and migration to terrestrial ecosystems.