Evolution of the F0F1 ATP Synthase Complex in Light of the Patchy Distribution of Different Bioenergetic Pathways across Prokaryotes

Abstract

Bacteria and archaea are characterized by an amazing metabolic diversity, which allows them to persist in diverse and often extreme habitats. Apart from oxygenic photosynthesis and oxidative phosphorylation, well-studied processes from chloroplasts and mitochondria of plants and animals, prokaryotes utilize various chemo- or lithotrophic modes, such as anoxygenic photosynthesis, iron oxidation and reduction, sulfate reduction, and methanogenesis. Most bioenergetic pathways have a similar general structure, with an electron transport chain composed of protein complexes acting as electron donors and acceptors, as well as a central cytochrome complex, mobile electron carriers, and an ATP synthase. While each pathway has been studied in considerable detail in isolation, not much is known about their relative evolutionary relationships. Wanting to address how this metabolic diversity evolved, we mapped the distribution of nine bioenergetic modes on a phylogenetic tree based on 16S rRNA sequences from 272 species representing the full diversity of prokaryotic lineages. This highlights the patchy distribution of many pathways across different lineages, and suggests either up to 26 independent origins or 17 horizontal gene transfer events. Next, we used comparative genomics and phylogenetic analysis of all subunits of the F0F1 ATP synthase, common to most bacterial lineages regardless of their bioenergetic mode. Our results indicate an ancient origin of this protein complex, and no clustering based on bioenergetic mode, which suggests that no special modifications are needed for the ATP synthase to work with different electron transport chains. Moreover, examination of the ATP synthase genetic locus indicates various gene rearrangements in the different bacterial lineages, ancient duplications of atpI and of the beta subunit of the F0 subcomplex, as well as more recent stochastic lineage-specific and species-specific duplications of all subunits. We discuss the implications of the overall pattern of conservation and flexibility of the F0F1 ATP synthase genetic locus.

pH determines the energetic efficiency of the cyanobacterial CO 2 concentrating mechanism

“…Here, we express the cost of fixation in units of H + gradient dissipation-the number of H + transported along the concentration gradient (i.e., the fundamental currency of the electrochemical potential). Cyanobacteria convert a proton gradient into ATP by means of the F 1 F o ATP synthase, which synthesizes one ATP for every four H + translocated (40,41). Active transport of Ci is the chief energetic cost associated with the CCM.…”

Evolution of b-type cytochromes in prokaryotes

“…272 species of bacteria and archaea, whose genomes have been completely sequenced and are available at NCBI, were chosen so as to cover the full diversity of bacterial and archaeal lineages (Wu et al, 2009) (http://tolweb.org/tree/) and the full bioenergetic diversity per lineage, as previously described (Koumandou and Kossida, 2014). For lineages with many sequenced genomes, the tree of (Wu et al, 2009) was used to pick species so as to cover as much phylogenetic diversity as possible with a limited number of species.…”

“…As previously reported, this set of species was chosen to represent all the major prokaryotic lineages as evenly as possible given the sequencing bias (e.g. for proteobacteria), as well as the full variety of bioenergetics pathways used by prokaryotes, (Koumandou and Kossida, 2014).…”

“…Much attention has been focused on the emergence of oxygenic photosynthesis, as this likely had far-reaching implications for life on Earth (Olson and Blankenship, 2004, Xiong, 2006, Blankenship, 2010. 16S rRNA phylogeny reveals a patchy picture of bioenergetic pathways in different taxonomic groups, suggestive of rampant horizontal gene transfer (HGT) (Castresana, 2001, Reysenbach and Shock, 2002, Boucher et al, 2003, Koumandou and Kossida, 2014. Molecular evolution studies of the electron transport chains of different pathways could help to clarify this picture.…”

“…Each pathway depends on an electron transport chain (ETC) which comprises protein complexes acting as electron donors and electron acceptors, with a cytochrome bc-type complex and mobile electron carriers between them; the ETC generates a proton gradient across the bioenergetic membrane which is then harnessed by the ATP synthase complex to generate ATP. Recently we reported that the ATP synthase from a variety of organisms, representing nine bioenergetic pathways, shows an ancient origin and no propensity to horizontal gene transfer (Koumandou and Kossida, 2014). Indeed, the evolution of the ATP synthase subunits closely follows taxonomic groups, indicating that there is not a special enzyme associated with each ETC.…”