Carbon fixation by marine ultra-small prokaryotes

Lannes, Romain; Olsson-Francis, Karen; Lopez, Philippe and Bapteste, Eric (2019). Carbon fixation by marine ultra-small prokaryotes. Genome Biology and Evolution, 11(4) pp. 1166–1177.

DOI: https://doi.org/10.1093/gbe/evz050

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. Nanoorganisms, 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 were quantified and tested for the presence of all key enzymes in a diversity of nanoorganisms across the World Ocean. The novel marine ultra-small prokaryotes was demonstrated to collectively harbor the genes required for carbon fixation, in particular the ‘energetically efficient’ DH pathway, and HBC pathways. This contrasted with the known carbon metabolic pathways associated with CPR memebers in aquifers, where they are described as degraders (Castelle 2015 et al., 2015, Castelle et al., 2018, Anantharaman et al., 2016). Our findings offer the possibility that nanoorganisms have a broader contribution to carbon fixation and cycling than currently assumed. Furthermore, CPR and DPANN are possibly not the only nanosized prokaryotes; therefore, the discovery of new autotrophic marine nanoorganisms, by future single cell genomics is anticipated.

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