Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces

Gabriela F. Paredes, Tobias Viehboeck, Raymond Lee, Marton Palatinszky, Michaela A. Mausz, Siegfried Reipert, Arno Schintlmeister, Andreas Maier, Jean Marie Volland, Claudia Hirschfeld, Michael Wagner, David Berry, Stephanie Markert, Silvia Bulgheresi*, Lena König

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

9 Citations (Scopus)
81 Downloads (Pure)

Abstract

Chemosynthetic symbioses occur worldwide in marine habitats, but comprehensive physiological studies of chemoautotrophic bacteria thriving on animals are scarce. Stilbonematinae are coated by thiotrophic Gammaproteobacteria. As these nematodes migrate through the redox zone, their ectosymbionts experience varying oxygen concentrations. However, nothing is known about how these variations affect their physiology. Here, by applying omics, Raman microspectroscopy, and stable isotope labeling, we investigated the effect of oxygen on "Candidatus Thiosymbion oneisti." Unexpectedly, sulfur oxidation genes were upregulated in anoxic relative to oxic conditions, but carbon fixation genes and incorporation of 13C-labeled bicarbonate were not. Instead, several genes involved in carbon fixation were upregulated under oxic conditions, together with genes involved in organic carbon assimilation, polyhydroxyalkanoate (PHA) biosynthesis, nitrogen fixation, and urea utilization. Furthermore, in the presence of oxygen, stress-related genes were upregulated together with vitamin biosynthesis genes likely necessary to withstand oxidative stress, and the symbiont appeared to proliferate less. Based on its physiological response to oxygen, we propose that "Ca. T. oneisti" may exploit anaerobic sulfur oxidation coupled to denitrification to proliferate in anoxic sand. However, the ectosymbiont would still profit from the oxygen available in superficial sand, as the energy-efficient aerobic respiration would facilitate carbon and nitrogen assimilation.

Original languageEnglish
Article numbere01186-20
JournalmSystems
Volume6
Issue number3
ISSN2379-5077
DOIs
Publication statusPublished - Jun 2021

Bibliographical note

Publisher Copyright:
© 2021 American Society for Microbiology. All rights reserved.

Keywords

  • Anoxia
  • Chemosynthesis
  • Gammaproteobacteria
  • Sulfur oxidation
  • Symbiosis
  • Thiosymbion
  • Thiotrophic bacteria

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