The metabolic network of the last bacterial common ancestor

Xavier, Joana C.; Gerhards, Rebecca E.; Wimmer, Jessica L. E.; Brueckner, Julia; Tria, Fernando D. K.; Martin, William

doi:10.1038/s42003-021-01918-4

Cited by 44 publications

(40 citation statements)

References 88 publications

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“…2, Table S1). More recently, and using different methods, LBCA has been reported as an anaerobic, rod-shaped cell utilising glucogenesis [84], and as rod shaped (with a diderm outer membrane), and motile [85], both studies depicting the bacterial ancestor in a very similar way to our own results.…”

Section: Resultssupporting

confidence: 81%

Phenotypic reconstruction of the last universal common ancestor reveals a complex cell

Baidouri

Venditti

Suzuki

et al. 2020

Preprint

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A fundamental concept in evolutionary theory is the last universal common ancestor (LUCA) from which all living organisms. While some authors have suggested a relatively complex LUCA it is still widely assumed that LUCA must have been a very simple cell and that life has subsequently increased in complexity through time. However, while current thought does tend towards a general increase in complexity through time in Eukaryotes, there is increasing evidence that bacteria and archaea have undergone considerable genome reduction during their evolution. This raises the surprising possibility that LUCA, as the ancestor of bacteria and archaea may have been a considerably complex cell. While hypotheses regarding the phenotype of LUCA do exist, all are founded on gene presence/absence. Yet, despite recent attempts to link genes and phenotypic traits in prokaryotes, it is still inherently difficult to predict phenotype based on the presence or absence of genes alone. In response to this, we used Bayesian phylogenetic comparative methods to predict ancestral traits. Testing for robustness to horizontal gene transfer (HGT) we inferred the phenotypic traits of LUCA using two robust published phylogenetic trees and a dataset of 3,128 bacterial and archaeal species (Supplementary Information). Our results depict LUCA as a far more complex cell than has previously been proposed, challenging the evolutionary model of increased complexity through time in prokaryotes. Given current estimates for the emergence of LUCA we suggest that early life very rapidly evolved considerable cellular complexity.

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Section: Resultssupporting

confidence: 81%

Phenotypic reconstruction of the last universal common ancestor reveals a complex cell

Baidouri

Venditti

Suzuki

et al. 2020

Preprint

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“…The topology of our phylogeny of the primary domains of life (Figure 6) is consistent with recent single-domain trees inferred for Archaea and Bacteria independently (Coleman et al, 2021;Dombrowski et al, 2020;Williams et al, 2017), although the deep relationships within Bacteria are only poorly resolved, with the exception of the monophyly of Gracilicutes (Figure 6). A recent analysis suggested that, among extant lineages, the metabolisms of Clostridia, Deltaproteobacteria, Actinobacteria and some Aquificae might best preserve the metabolism of the last bacterial common ancestor (Xavier et al, 2021). Assuming a universal root between Archaea and Bacteria (Dagan et al, 2010;Gogarten et al, 1989;Iwabe et al, 1989), none of these groups branch near the bacterial root in our analysis (Figure 6).…”

Section: A Phylogeny Of Archaea and Bacteria Inferred From 27 Vertically-evolving Marker Genesmentioning

confidence: 83%

An estimate of the deepest branches of the tree of life from ancient vertically-evolving genes

Moody

Mahendrarajah

Dombrowski

et al. 2021

Preprint

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The tree of life is generally estimated from a core set of 16-56 genes coding for proteins predominantly involved in translation and other conserved informational and cellular processes. These markers represent only a fraction of the genes that were likely present in the last universal common ancestor (LUCA), but are useful for deep phylogenetic reconstructions because their mode of inheritance appears to be mainly vertical, which satisfies the assumptions of gene concatenation and supertree methods. Previous phylogenetic analyses of these genes recovered a long branch between Archaea and Bacteria. By contrast, a recent study made use of a greatly expanded set of 381 marker genes and recovered a much shorter branch length between Archaea and Bacteria, comparable to some divergences within the domains. These analyses suggest that the apparent deep split between Archaea and Bacteria may be the result of accelerated evolution of ribosomal genes. Here we re-evaluate the evolutionary history of the expanded marker gene set and show that substitutional saturation, inter-domain gene transfer, hidden paralogy, and poor model fit contribute to the inference of an artificially shortened inter-domain branch. Our results do not exclude a moderately faster rate of ribosomal gene evolution during the divergence of Archaea and Bacteria, but indicate that vertically-evolving marker genes across all functional categories support a major genetic divergence between the two primary domains of life.

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“…Though the remaining chemical reactions of the core do not occur in all genomes, as auxotrophies arise recurrently in evolution, they are universal at the level of primary production, the process that has fueled all ecosystems from origins to today ( Hamilton et al, 2016 ; Martin et al, 2018 ). However, the enzymes that catalyze the reactions of the core are not universal, such that the core cannot be identified through purely genomic comparisons because (i) reactions that arose post LUCA , in particular O 2 -dependent reactions ( Dailey et al, 2017 ; Jabłońska and Tawfik, 2021 ), need to be filtered out ( Wimmer et al, 2021a ), (ii) because lateral gene transfers of recently arisen pathways have to be filtered out ( Weiss et al, 2016 ), and (iii) because the enzymes that catalyze these reactions are often unrelated across the archaeal-bacterial divide ( Sousa et al, 2013 ), suggesting independent origins of enzymatic pathways from LUCA en route to the last common ancestors of archaea ( Williams et al, 2017 ) and bacteria ( Xavier et al, 2021 ), respectively.…”

Section: Introductionmentioning

confidence: 99%

Energy at Origins: Favorable Thermodynamics of Biosynthetic Reactions in the Last Universal Common Ancestor (LUCA)

et al. 2021

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Though all theories for the origin of life require a source of energy to promote primordial chemical reactions, the nature of energy that drove the emergence of metabolism at origins is still debated. We reasoned that evidence for the nature of energy at origins should be preserved in the biochemical reactions of life itself, whereby changes in free energy, ΔG, which determine whether a reaction can go forward or not, should help specify the source. By calculating values of ΔG across the conserved and universal core of 402 individual reactions that synthesize amino acids, nucleotides and cofactors from H2, CO2, NH3, H2S and phosphate in modern cells, we find that 95–97% of these reactions are exergonic (ΔG ≤ 0 kJ⋅mol−1) at pH 7-10 and 80-100°C under nonequilibrium conditions with H2 replacing biochemical reductants. While 23% of the core’s reactions involve ATP hydrolysis, 77% are ATP-independent, thermodynamically driven by ΔG of reactions involving carbon bonds. We identified 174 reactions that are exergonic by –20 to –300 kJ⋅mol−1 at pH 9 and 80°C and that fall into ten reaction types: six pterin dependent alkyl or acyl transfers, ten S-adenosylmethionine dependent alkyl transfers, four acyl phosphate hydrolyses, 14 thioester hydrolyses, 30 decarboxylations, 35 ring closure reactions, 31 aromatic ring formations, and 44 carbon reductions by reduced nicotinamide, flavins, ferredoxin, or formate. The 402 reactions of the biosynthetic core trace to the last universal common ancestor (LUCA), and reveal that synthesis of LUCA’s chemical constituents required no external energy inputs such as electric discharge, UV-light or phosphide minerals. The biosynthetic reactions of LUCA uncover a natural thermodynamic tendency of metabolism to unfold from energy released by reactions of H2, CO2, NH3, H2S, and phosphate.

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The metabolic network of the last bacterial common ancestor

Cited by 44 publications

References 88 publications

Phenotypic reconstruction of the last universal common ancestor reveals a complex cell

Phenotypic reconstruction of the last universal common ancestor reveals a complex cell

An estimate of the deepest branches of the tree of life from ancient vertically-evolving genes

Energy at Origins: Favorable Thermodynamics of Biosynthetic Reactions in the Last Universal Common Ancestor (LUCA)

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