TY - JOUR
T1 - Anaerobic sulfur oxidation underlies adaptation of a chemosynthetic symbiont to oxic-anoxic interfaces
AU - Paredes, Gabriela F.
AU - Viehboeck, Tobias
AU - Lee, Raymond
AU - Palatinszky, Marton
AU - Mausz, Michaela A.
AU - Reipert, Siegfried
AU - Schintlmeister, Arno
AU - Maier, Andreas
AU - Volland, Jean Marie
AU - Hirschfeld, Claudia
AU - Wagner, Michael
AU - Berry, David
AU - Markert, Stephanie
AU - Bulgheresi, Silvia
AU - König, Lena
N1 - Publisher Copyright:
© 2021 American Society for Microbiology. All rights reserved.
PY - 2021/6
Y1 - 2021/6
N2 - 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.
AB - 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.
KW - Anoxia
KW - Chemosynthesis
KW - Gammaproteobacteria
KW - Sulfur oxidation
KW - Symbiosis
KW - Thiosymbion
KW - Thiotrophic bacteria
UR - http://www.scopus.com/inward/record.url?scp=85107422933&partnerID=8YFLogxK
U2 - 10.1128/mSystems.01186-20
DO - 10.1128/mSystems.01186-20
M3 - Journal article
AN - SCOPUS:85107422933
SN - 2379-5077
VL - 6
JO - mSystems
JF - mSystems
IS - 3
M1 - e01186-20
ER -