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.IMPORTANCE Chemoautotrophic endosymbionts are famous for exploiting sulfur oxidization to feed marine organisms with fixed carbon. However, the physiology of thiotrophic bacteria thriving on the surface of animals (ectosymbionts) is less understood. One longstanding hypothesis posits that attachment to animals that migrate between reduced and oxic environments would boost sulfur oxidation, as the ectosymbionts would alternatively access sulfide and oxygen, the most favorable electron acceptor. Here, we investigated the effect of oxygen on the physiology of “Candidatus Thiosymbion oneisti,” a gammaproteobacterium which lives attached to marine nematodes inhabiting shallow-water sand. Surprisingly, sulfur oxidation genes were upregulated under anoxic relative to oxic conditions. Furthermore, under anoxia, the ectosymbiont appeared to be less stressed and to proliferate more. We propose that animal-mediated access to oxygen, rather than enhancing sulfur oxidation, would facilitate assimilation of carbon and nitrogen by the ectosymbiont.
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.IMPORTANCE Chemoautotrophic endosymbionts are famous for exploiting sulfur oxidization to feed marine organisms with fixed carbon. However, the physiology of thiotrophic bacteria thriving on the surface of animals (ectosymbionts) is less understood. One longstanding hypothesis posits that attachment to animals that migrate between reduced and oxic environments would boost sulfur oxidation, as the ectosymbionts would alternatively access sulfide and oxygen, the most favorable electron acceptor. Here, we investigated the effect of oxygen on the physiology of “Candidatus Thiosymbion oneisti,” a gammaproteobacterium which lives attached to marine nematodes inhabiting shallow-water sand. Surprisingly, sulfur oxidation genes were upregulated under anoxic relative to oxic conditions. Furthermore, under anoxia, the ectosymbiont appeared to be less stressed and to proliferate more. We propose that animal-mediated access to oxygen, rather than enhancing sulfur oxidation, would facilitate assimilation of carbon and nitrogen by the ectosymbiont.
KW - AZOSPIRILLUM-BRASILENSE
KW - BACTERIAL-CELLS
KW - CARBON FIXATION
KW - CHEMOAUTOTROPHIC SYMBIONTS
KW - ESCHERICHIA-COLI
KW - FATTY-ACIDS
KW - Gammaproteobacteria
KW - MARINE NEMATODES
KW - NITRATE RESPIRATION
KW - SP-NOV
KW - SULFIDE SYSTEM
KW - Thiosymbion
KW - anoxia
KW - chemosynthesis
KW - sulfur oxidation
KW - symbiosis
KW - thiotrophic bacteria
KW - Symbiosis
KW - Anoxia
KW - Sulfur oxidation
KW - Thiotrophic bacteria
KW - Chemosynthesis
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 - Article
C2 - 34058098
SN - 2379-5077
VL - 6
JO - mSystems
JF - mSystems
IS - 3
M1 - e01186-20
ER -