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 ((Formula presented.))-reduction processes. Denitrification was the dominant pathway of (Formula presented.) reduction (>90%), primarily fuelled by (Formula presented.) from bottom water. In addition to pumping (Formula presented.) -rich bottom water within the burrows, chironomid larvae host microbiota capable of (Formula presented.) reduction. However, the contribution of larval microbiota is lower than that of microbes inhabiting the burrow walls. Interestingly, dinitrogen fixation co-occurred with (Formula presented.) reduction processes, indicating versatility of the larvae's microbial community. Assuming all larvae (averaging 1,800 ind./m2) leave the sediment following metamorphosis into flying adults, we estimated a displacement of 47,787 µmol of organic N/m2 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.