Horizontal acquisition of a patchwork Calvin cycle by symbiotic and free-living Campylobacterota (formerly Epsilonproteobacteria)

Abstract

36Although the majority of known autotrophs use the Calvin-Benson-Bassham (CBB) cycle for 37 carbon fixation, all currently described autotrophs from the Campylobacterota (previously 38 Epsilonproteobacteria) use the reductive tricarboxylic acid cycle (rTCA) instead. We 39 discovered campylobacterotal epibionts ("Candidatus Thiobarba") of deep-sea mussels that 40 have acquired a complete CBB cycle and lost key genes of the rTCA cycle. Intriguingly, the 41 phylogenies of campylobacterotal CBB genes suggest they were acquired in multiple 42 transfers from Gammaproteobacteria closely related to sulfur-oxidizing endosymbionts 43 associated with the mussels, as well as from Betaproteobacteria. We hypothesize that 44 "Ca. Thiobarba" switched from the rTCA to a fully functional CBB cycle during its evolution, 45 by acquiring genes from multiple sources, including co-occurring symbionts. We also found 46 key CBB cycle genes in free-living Campylobacterota, suggesting that the CBB cycle may be 47 more widespread in this phylum than previously known. Metatranscriptomics and 48 metaproteomics confirmed high expression of CBB cycle genes in mussel-associated 49 "Ca. Thiobarba". Direct stable isotope fingerprinting showed that "Ca. Thiobarba" has typical 50 CBB signatures, additional evidence that it uses this cycle for carbon fixation. Our discovery 51 calls into question current assumptions about the distribution of carbon fixation pathways 52 across the tree of life, and the interpretation of stable isotope measurements in the 53 environment. 54 55All life on earth is based on carbon fixation, and its molecular machinery is increasingly 56 becoming a focus of biotechnology and geo-engineering efforts due to its potential to 57 improve crop yields and sequester carbon dioxide from the atmosphere 1 . Seven carbon 58 fixation pathways have evolved in nature, and one purely synthetic pathway runs in vitro [2][3][4] . 59Of the six natural pathways, the Calvin-Benson-Bassham (CBB) cycle was the first 60 discovered, and is believed to be the most widespread 5-7 . The CBB cycle is used by a 61 diverse array of organisms throughout the tree of life, including plants and algae, 62 cyanobacteria, and autotrophic members of the Alpha-, Beta-and Gammaproteobacteria. Its 63 key enzyme, the ribulose bisphosphate carboxylase/oxygenase (RuBisCO) is thought to be 64 the most abundant, as well as one of the most ancient enzymes on Earth 8,9 . 65 The reductive tricarboxylic acid (rTCA) cycle was the second described carbon fixation 66 pathway 10 . In short, it is a reversal of the energy-generating and oxidative TCA cycle. Instead 67 of oxidizing acetyl-CoA and generating ATP and reducing equivalents, it reduces CO2 at the 68 expense of ATP and reducing equivalents 2,7,10 . Most of the enzymes are shared with the TCA 69 cycle, except for those that catalyze irreversible reactions in the TCA, such as citrate 70 synthase, which is catalyzed by ATP citrate lyase in the rTCA. However, given sufficiently 71 high reactant to product ratios and ...

An Aerobic Anoxygenic Phototrophic Bacterium Fixes CO2via the Calvin-Benson-Bassham Cycle

“…As the presence of puf genes, which encode bacterial reaction centre subunits, and genes necessary for bacteriochlorophyll biosynthesis in the PGC suggests, strain B3 may carry out a phototrophic strategy with type II reaction centres. [14]. None of pathways except CBB has been identified in strain B3.…”

“…Carbon fixation provides the basis for all life on Earth [13], and seven carbon fixation pathways have evolved in nature [14]. Among the seven pathways, the Calvin-Benson-Bassham (CBB) cycle is the most widespread [15] and responsible for the most carbon fixation on Earth [16].…”

Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO 2 Fixation

“…Indeed, several host groups have become so completely dependent on their symbionts for nutrition that they have reduced digestive systems. All sulfur-oxidizing symbioses investigated thus far possess a primary thiotrophic symbiont with genes of either the Calvin-Benson-Bassham (CBB) (3–10) or reverse tricarboxylic acid (rTCA) (11, 12) cycle for CO 2 fixation, and the different pathways may relate to different ecological niches occupied by the symbioses (13). The symbionts of the vestimentiferan tubeworms are additionally able to encode both the CBB and rTCA cycles, which may be active under different environmental conditions (14–16).…”

CaveThiovulaceaediffer metabolically and genomically from marine species

“…Such depletion in 13 C is rather typical of organisms utilizing the Calvin-Benson-Bassham (CBB) cycle (Pearson, 2010). Recently it was discovered that some Campylobacterota lost the genes needed for the TCA in favor of a gradual acquisition of those required for the CBB cycle (Assié et al , 2020). Most of the genes involved in the CBB cycle are common in heterotrophs as well being part of alternative reactions.…”