Abstract
Autotrophic carbon fixation is a crucial process for sustaining life on Earth. To date, six pathways, the Calvin–Benson–Bassham cycle, the reductive tricarboxylic acid cycle, the 3-hydroxypropionate bi-cycle, the Wood–Ljungdahl pathway, the dicarboxylate/4-hydroxybutyrate cycle, and the 4-hydroxybutyrate cycle, have been described. Nano-organisms such as members of the Candidate Phyla Radiation (CPR) bacterial superphylum and the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohalorchaeota (DPANN) archaeal superphylum could deeply impact carbon cycling and carbon fixation in ways that are still to be determined. CPR and DPANN are ubiquitous in the environment but understudied; their gene contents are not exhaustively described; and their metabolisms are not yet fully understood. Here, the completeness of each of the above pathways was quantified and tested for the presence of all key enzymes in nano-organisms from across the World Ocean. The novel marine ultrasmall prokaryotes were demonstrated to collectively harbor the genes required for carbon fixation, in particular the “energetically efficient” dicarboxylate/4-hydroxybutyrate pathway and the 4-hydroxybutyrate pathway. This contrasted with the known carbon metabolic pathways associated with CPR members in aquifers, where they are described as degraders (Castelle CJ, et al. 2015. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol. 25(6):690–701; Castelle CJ, et al. 2018. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat Rev Microbiol. 16(10):629–645; Anantharaman K, et al. 2016. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 7:13219.). Our findings suggest that nano-organisms have a broader contribution to carbon fixation and cycling than currently assumed. Furthermore, CPR and DPANN superphyla are possibly not the only nanosized prokaryotes; therefore, the discovery of new autotrophic marine nano-organisms by future single cell genomics is anticipated.
Highlights
Autotrophic carbon fixation is a crucial process for sustaining life on Earth as it fixes inorganic carbon, including the sequestration of atmospheric carbon dioxide (De La Rocha and Passow 2014), into organic carbon (Hugler and Sievert 2011)
Twenty thousand three hundred sixty-eight environmental homologs sequences were identified for six autotrophic carbon fixation pathways, at a threshold of sequence identity >25%, of mutual coverage >70%, and E-value
With respect to the original data sets associated with the ultrasmall size fraction of the TARA OCEANS project, the “cleaned” data sets developed in this study were significantly enriched in taxonomically unclassified sequences, and in Candidate Phyla Radiation (CPR) and DPANN sequences
Summary
Autotrophic carbon fixation is a crucial process for sustaining life on Earth as it fixes inorganic carbon, including the sequestration of atmospheric carbon dioxide (De La Rocha and Passow 2014), into organic carbon (Hugler and Sievert 2011). It is responsible for the annually net fixation of 7 Â 1016 g carbon, which corresponds to the conservation of 2.8 Â 1018 kJ of energy (Berg 2011). An increasing number of models have been developed that highlight the role of micro-organisms in carbon fixation
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