Abstract
Most autotrophs use the Calvin–Benson–Bassham (CBB) cycle for carbon fixation. In contrast, all currently described autotrophs from the Campylobacterota (previously Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We discovered campylobacterotal epibionts (“Candidatus Thiobarba”) of deep-sea mussels that have acquired a complete CBB cycle and may have lost most key genes of the rTCA cycle. Intriguingly, the phylogenies of campylobacterotal CBB cycle genes suggest they were acquired in multiple transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts associated with the mussels, as well as from Betaproteobacteria. We hypothesize that “Ca. Thiobarba” switched from the rTCA cycle to a fully functional CBB cycle during its evolution, by acquiring genes from multiple sources, including co-occurring symbionts. We also found key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be more widespread in this phylum than previously known. Metatranscriptomics and metaproteomics confirmed high expression of CBB cycle genes in mussel-associated “Ca. Thiobarba”. Direct stable isotope fingerprinting showed that “Ca. Thiobarba” has typical CBB signatures, suggesting that it uses this cycle for carbon fixation. Our discovery calls into question current assumptions about the distribution of carbon fixation pathways in microbial lineages, and the interpretation of stable isotope measurements in the environment.
Highlights
These authors contributed : Adrien Assié, Nikolaus Leisch
The draft genomes had an average nucleotide sequence identity (ANI) of 83.1%, indicating that they represent different species likely belonging to the same genus [39,40,41,42]
The distribution of gammaproteobacterial and campylobacterotal sulfur oxidizers is a typical example of adaptation to geochemical niches in a range of environments from hydrothermal vents [23] and cold seeps [21] to oxygen minimum zones [76] and coastal sediments [77]
Summary
Carbon fixation by chemoautotrophic microorganisms forms the basis of entire ecosystems at deep-sea hydrothermal vents and cold seeps [15, 16] Most of this carbon is fixed either via the CBB cycle, used by many gammaproteobacterial autotrophs, or the rTCA cycle, used by campylobacterotal autotrophs. Some sulfur-oxidizing symbionts use hydrogen as an energy source, and some mussel species host additional symbionts that gain energy from short-chain alkanes [32, 33] In addition to these dominant endosymbionts, Assié et al recently discovered epibionts that colonize bathymodiolin mussels from around the world [34]. The discovery of Campylobacterota that use the CBB cycle for CO2 fixation has implications for understanding the evolution of carbon fixation pathways, and for interpreting stable isotope values in environmental samples
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