Take my breath away: anoxia enhances sulfur-driven chemosynthesis in nematode symbionts

Gabriela Fabiola Paredes Rojas, Tobias Viehböck, Jean-Marie Volland, Raymond Lee, Silvia Bulgheresi

Stilbonematinae are free-living marine nematodes that live in symbiotic association with Thiosymbion Gammaproteobacteria, a monophyletic group of autotrophic sulfur-oxidizers. These possess the genetic repertoire to drive CO2 fixation through the oxidation of reduced sulfur compounds. Despite the fact that they may occur at extremely high abundances (>105 per m2) in shallow water sediments and can hence affect their biogeochemistry, the raison d'être of these symbioses is still eluding us. It has long been hypothesized that the symbionts associate with the nematodes to exploit their vertical migrations through the redox zone that is to alternatively access oxygen (e- acceptor) in the upper sand layers and sulfide (e- donor) in the deeper ones. Additionally, it has been hypothesized that the ability of using nitrate as an alternative electron acceptor (denitrification) might stimulate the oxidation of sulfide in anoxic sediment layers. However, these hypotheses have not been tested so far. Here, we assessed the effect of oxygen on sulfur-driven chemosynthesis by (1) quantifying the transcription of key metabolic genes (i.e. norB, aprA, dsrA, cbbL) by qPCR and (2) by measuring the incorporation of isotopically labelled NaHCO3 (13C) under oxic and anoxic conditions. We showed that C fixation, denitrification and S oxidation genes were upregulated in anoxic relative to oxic conditions. Moreover, mass spectrometric analysis of 13C incorporation indicated higher CO2 fixation rates in anoxic conditions. All in all, our data suggest that denitrification fuels stilbonematid symbiont metabolism and that this is optimized to exploit anoxic environments. Consistently, according to the presented in situ nematode distribution >97% of a given species’ population thrives at O2 concentration below 10 µM. In conclusion, our data indicate that sulfur oxidation-driven chemosynthesis does not require nematode migrations through the O2/H2S redox layer. To unravel alternative roles of the host in symbiont metabolism, dual comparative RNA seq is ongoing.

Department für Ökogenomik und Systembiologie
Externe Organisation(en)
Washington State University
ÖFOS 2012
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