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Bioenergetic evolution in proteobacteria and mitochondria.

ABSTRACT: Mitochondria are the energy-producing organelles of our cells and derive from bacterial ancestors that became endosymbionts of microorganisms from a different lineage, together with which they formed eukaryotic cells. For a long time it has remained unclear from which bacteria mitochondria actually evolved, even if these organisms in all likelihood originated from the ? lineage of proteobacteria. A recent article (Degli Esposti M, et al. 2014. Evolution of mitochondria reconstructed from the energy metabolism of living bacteria. PLoS One 9:e96566) has presented novel evidence indicating that methylotrophic bacteria could be among the closest living relatives of mitochondrial ancestors. Methylotrophs are ubiquitous bacteria that live on single carbon sources such as methanol and methane; in the latter case they are called methanotrophs. In this review, I examine their possible ancestry to mitochondria within a survey of the common features that can be found in the central and terminal bioenergetic systems of proteobacteria and mitochondria. I also discuss previously overlooked information on methanotrophic bacteria, in particular their intracytoplasmic membranes resembling mitochondrial cristae and their capacity of establishing endosymbiotic relationships with invertebrate animals and archaic plants. This information appears to sustain the new idea that mitochondrial ancestors could be related to extant methanotrophic proteobacteria, a possibility that the genomes of methanotrophic endosymbionts will hopefully clarify.

SUBMITTER: Degli Esposti M

PROVIDER: S-EPMC4986455 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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Bioenergetic evolution in proteobacteria and mitochondria.

Degli Esposti Mauro M

Genome biology and evolution 20141127 12

Mitochondria are the energy-producing organelles of our cells and derive from bacterial ancestors that became endosymbionts of microorganisms from a different lineage, together with which they formed eukaryotic cells. For a long time it has remained unclear from which bacteria mitochondria actually evolved, even if these organisms in all likelihood originated from the α lineage of proteobacteria. A recent article (Degli Esposti M, et al. 2014. Evolution of mitochondria reconstructed from the ene ...[more]

PMID: 25432941

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Project description:BackgroundThe effectiveness of elimination of slightly deleterious mutations depends mainly on drift and recombination frequency. Here we analyze the influence of these two factors on the strength of the purifying selection in mitochondrial and proteobacterial orthologous genes taking into account the differences in the organism lifestyles.Results(I) We found that the probability of fixation of nonsynonymous substitutions (Kn/Ks) in mitochondria is significantly lower compared to obligate intracellular bacteria and even marginally significantly lower compared to free-living bacteria. The comparison of bacteria of different lifestyles demonstrates more effective elimination of slightly deleterious mutations in (II) free-living bacteria as compared to obligate intracellular species and in (III) obligate intracellular parasites as compared to obligate intracellular symbionts. (IV) Finally, we observed that the level of the purifying selection (i.e. 1-Kn/Ks) increases with the density of mobile elements in bacterial genomes.ConclusionThis study shows that the comparison of patterns of molecular evolution of orthologous genes between ecologically different groups of organisms allow to elucidate the genetic consequences of their various lifestyles. Comparing the strength of the purifying selection among proteobacteria with different lifestyles we obtained results, which are in concordance with theoretical expectations: (II) low effective population size and level of recombination in obligate intracellular proteobacteria lead to less effective elimination of mutations compared to free-living relatives; (III) rare horizontal transmissions, i.e. effectively zero recombination level in symbiotic obligate intracellular bacteria leads to less effective purifying selection than in parasitic obligate intracellular bacteria; (IV) the increased frequency of recombination in bacterial genomes with high mobile element density leads to a more effective elimination of slightly deleterious mutations. At the same time, (I) more effective purifying selection in relatively small populations of nonrecombining mitochondria as compared to large populations of recombining proteobacteria was unexpected. We hypothesize that additional features such as the high number of protein-protein interactions or female germ-cell atresia increase evolutionary constraints and maintain the effective purifying selection in mitochondria, but more work is needed to definitely establish these additional features.

Project description:Although prokaryotes are usually classified using molecular phylogenies instead of phenotypes after the advent of gene sequencing, neither of these methods is satisfactory because the phenotypes cannot explain the molecular trees and the trees do not fit the phenotypes. This scientific crisis still exists and the profound disconnection between these two pillars of evolutionary biology--genotypes and phenotypes--grows larger. We use rings and a genomic form of goods thinking to resolve this conundrum (McInerney JO, Cummins C, Haggerty L. 2011. Goods thinking vs. tree thinking. Mobile Genet Elements. 1:304-308; Nelson-Sathi S, et al. 2015. Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517:77-80). The Proteobacteria is the most speciose prokaryotic phylum known. It is an ideal phylogenetic model for reconstructing Earth's evolutionary history. It contains diverse free living, pathogenic, photosynthetic, sulfur metabolizing, and symbiotic species. Due to its large number of species (Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: the unseen majority. Proc Nat Acad Sci U S A. 95:6578-6583) it was initially expected to provide strong phylogenetic support for a proteobacterial tree of life. But despite its many species, sequence-based tree analyses are unable to resolve its topology. Here we develop new rooted ring analyses and study proteobacterial evolution. Using protein family data and new genome-based outgroup rooting procedures, we reconstruct the complex evolutionary history of the proteobacterial rings (combinations of tree-like divergences and endosymbiotic-like convergences). We identify and map the origins of major gene flows within the rooted proteobacterial rings (P < 3.6 × 10(-6)) and find that the evolution of the "Alpha-," "Beta-," and "Gammaproteobacteria" is represented by a unique set of rings. Using new techniques presented here we also root these rings using outgroups. We also map the independent flows of genes involved in DNA-, RNA-, ATP-, and membrane- related processes within the Proteobacteria and thereby demonstrate that these large gene flows are consistent with endosymbioses (P < 3.6 × 10(-9)). Our analyses illustrate what it means to find that a gene is present, or absent, within a gene flow, and thereby clarify the origin of the apparent conflicts between genotypes and phenotypes. Here we identify the gene flows that introduced photosynthesis into the Alpha-, Beta-, and Gammaproteobacteria from the common ancestor of the Actinobacteria and the Firmicutes. Our results also explain why rooted rings, unlike trees, are consistent with the observed genotypic and phenotypic relationships observed among the various proteobacterial classes. We find that ring phylogenies can explain the genotypes and the phenotypes of biological processes within large and complex groups like the Proteobacteria.

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Bioenergetic evolution in proteobacteria and mitochondria.

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Bioenergetic evolution in proteobacteria and mitochondria.

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