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

Abstract

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./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.

Partitioning benthic nitrogen cycle processes among three common macrofauna holobionts

“…Single animal incubations allowed to quantify the direct contribution of macrofauna to O 2 respiration, which corresponded to nearly 22% of the total benthic O 2 uptake, within the range of 12-25% reported for other marine and coastal systems (Piepenburg et al 1995;Glud et al 2003;Politi et al 2021). Marenzelleria spp.…”

“…Individual incubations were employed to assess N-cycling pathways associated with the animal's holobionts. Incubations were carried out reproducing the experimental setup previously described in Marzocchi et al (2021) and Politi et al (2021). Briefly, animals were incubated in small bottom-capped Plexiglas cylindrical microcosms (total volume 227 ± 3 mL) partly filled with sterilized glass beads (Ø 1-1.3 mm; 4 mL-for M. affinis, 5 mL-for L. balthica, and 16 mL-for Marenzelleria spp.…”

“…Recent biogeochemical studies revealed for example how macrofauna-microbe holobionts might contribute to various processes of benthic N cycle, increasing its import, recycling and bioavailability to primary producers (Zilius et al 2020;Marzocchi et al 2021). Increasing synergy between molecular tools and the use of stable isotope probing have allowed large improvements in our understanding of elements cycling in holobionts and benthic macrofauna bioturbated sediments (Poulsen et al 2014;Vasquez-Cardenas et al 2016;Cardini et al 2019;Zilius et al 2020;Marzocchi et al 2021;Politi et al 2021).…”

“…Therefore, in macrofauna bioturbated sediments, the abundance and the activity of microbial communities often exceed those of surrounding, non-bioturbated sediments (Gilbertson et al 2012;Laverock et al 2014;Yazdani Foshtomi et al 2018;Samuiloviene et al 2019). The exterior body of macrofauna or its digestive system offer additional habitats for microbial communities, which are actively involved in different N-cycling pathways, such as nitrification, denitrification and dissimilatory nitrate reduction to ammonium (DNRA) or dinitrogen (N 2 ) fixation (Ray et al 2019;Zilius et al 2020;Marzocchi et al 2021;Politi et al 2021).…”

The Interplay of Macrofauna Functional Groups Shapes Nitrogen Cycling in Oligotrophic Estuarine Sediments

“…Denitri cation rates in animal holobionts from the Öre estuary were at least 66% higher than those measured at similar temperatures in chironomid larvae (C. plumosus; Politi et al 2021). Added tracer concentrations markedly differed between these two experiments, with 2-fold higher concentrations in C.…”