NanoSIMS and tissue autoradiography reveal symbiont carbon fixation and organic carbon transfer to giant ciliate host
2018
The giant colonial
ciliate
Zoothamnium niveumharbors a monolayer of the
gammaproteobacteria
Cand. Thiobios zoothamnicoli on its outer surface. Cultivation experiments revealed maximal growth and survival under steady flow of high oxygen and low sulfide concentrations. We aimed at directly demonstrating the
sulfur-oxidizing, chemoautotrophic nature of the symbionts and at investigating putative carbon transfer from the symbiont to the
ciliatehost. We performed pulse-chase incubations with 14C- and 13C-labeled bicarbonate under varying environmental conditions. A combination of tissue autoradiography and
nanoscale secondary ion mass spectrometrycoupled with transmission electron microscopy was used to follow the fate of the radioactive and stable
isotopesof
carbon, respectively. We show that symbiont cells fix substantial amounts of inorganic carbon in the presence of sulfide, but also (to a lesser degree) in the absence of sulfide by utilizing internally stored sulfur.
Isotope labelingpatterns point to translocation of organic carbon to the host through both release of these compounds and digestion of symbiont cells. The latter mechanism is also supported by ultracytochemical detection of acid phosphatase in lysosomes and in
food vacuolesof
ciliatecells. Fluorescence in situ hybridization of freshly collected
ciliatesrevealed that the vast majority of ingested microbial cells were ectosymbionts.
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