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Abstract:
Very few bacteria are able to fix carbon via both the reverse
tricarboxylic acid (rTCA) and the Calvin-Benson-Bassham (CBB) cycles,
such as symbiotic, sulfur-oxidizing bacteria that are the sole carbon
source for the marine tubeworm Riftia pachyptila, the fastest-growing
invertebrate. To date, the coexistence of these two carbon fixation
pathways had not been found in a cultured bacterium and could thus not
be studied in detail. Moreover, it was not clear if these two pathways
were encoded in the same symbiont individual, or if two symbiont
populations, each with one of the pathways, coexisted within tubeworms.
With comparative genomics, we show that Thioflavicoccus mobilis, a
cultured, free-living gam maproteobacterial sulfur oxidizer, possesses
the genes for both carbon fixation pathways. Here, we also show that
both the CBB and rTCA pathways are likely encoded in the genome of the
sulfur-oxidizing symbiont of the tubeworm Escarpia laminata from
deep-sea asphalt volcanoes in the Gulf of Mexico. Finally, we provide
genomic and transcriptomic data suggesting a potential electron flow
toward the rTCA cycle carboxylase 2-oxoglutarate:ferredoxin
oxidoreductase, via a rare variant of NADH dehydrogenase/heterodisulfide
reductase in the E. laminata symbiont. This electron-bifurcating
complex, together with NAD(P)(+) transhydrogenase and Na+ translocating
Rnf membrane complexes, may improve the efficiency of the rTCA cycle in
both the symbiotic and the free-living sulfur oxidizer.
IMPORTANCE Primary production on Earth is dependent on autotrophic
carbon fixation, which leads to the incorporation of carbon dioxide into
biomass. Multiple metabolic pathways have been described for autotrophic
carbon fixation, but most autotrophic organisms were assumed to have the
genes for only one of these pathways. Our finding of a cultivable
bacterium with two carbon fixation pathways in its genome, the rTCA and
the CBB cycle, opens the possibility to study the potential benefits of
having these two pathways and the interplay between them. Additionally,
this will allow the investigation of the unusual and potentially very
efficient mechanism of electron flow that could drive the rTCA cycle in
these autotrophs. Such studies will deepen our understanding of carbon
fixation pathways and could provide new avenues for optimizing carbon
fixation in biotechnological applications.
