How energy flow shapes cell evolution

Lane, Nick

doi:10.1016/j.cub.2020.03.055

Cited by 34 publications

(34 citation statements)

References 42 publications

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“…Eukaryotic genome size expansion was favoured by the acquisition of an endosymbiont, which evolved into the mitochondrion. This released bioenergetic constraints on cell size and allowed the evolution of genetic and morphological complexity ( Lane and Martin, 2010 ; Lane, 2014 ; Lane, 2020 ). The endosymbionts underwent gene loss, a frequently observed process in extant endosymbiotic relationships ( López-Madrigal and Gil, 2017 ) and transferred multiple genes to the host, enriching the host’s genome size with genes of proto-mitochondrial origin ( Timmis et al, 2004 ; Martin et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

“…Phylogenomic analysis shows that eukaryotes arose from the endosymbiosis between an archaeal host and a bacterial endosymbiont, the ancestor of mitochondria ( Müller et al, 2012 ; Williams et al, 2013 ; Martin et al, 2015 ; Zaremba-Niedzwiedzka et al, 2017 ). The presence of energy-producing endosymbionts allowed the first eukaryotes to escape the bioenergetic constraints that limit the genome size and cellular complexity of prokaryotes ( Lane and Martin, 2010 ; Lane, 2020 ). Extra energetic availability came with the evolutionary challenge of the coexistence of two different genomes within the same organism.…”

Section: Introductionmentioning

confidence: 99%

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Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Colnaghi

Lane

Pomiankowski

2020

eLife

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Prokaryotes acquire genes from the environment via lateral gene transfer (LGT). Recombination of environmental DNA can prevent the accumulation of deleterious mutations, but LGT was abandoned by the first eukaryotes in favour of sexual reproduction. Here we develop a theoretical model of a haploid population undergoing LGT which includes two new parameters, genome size and recombination length, neglected by previous theoretical models. The greater complexity of eukaryotes is linked with larger genomes and we demonstrate that the benefit of LGT declines rapidly with genome size. The degeneration of larger genomes can only be resisted by increases in recombination length, to the same order as genome size – as occurs in meiosis. Our results can explain the strong selective pressure towards the evolution of sexual cell fusion and reciprocal recombination during early eukaryotic evolution – the origin of meiotic sex.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Colnaghi

Lane

Pomiankowski

2020

eLife

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“…There are several defining differences comparing Archaea and Bacteria: i.e., (1) evolution of TFB (Archaea) versus σ factors (Bacteria); (2) utilization of DNAPs PolD and PolB (Archaea) versus PolC (Bacteria) ( Koonin et al, 2020 ), and (3) archaeal versus bacterial membranes ( Lane and Martin, 2012 ; Lane, 2020 ). Above, we have discussed the divergence of archaeal and bacterial GTFs and promoters in some detail.…”

Section: Divergence Of Archaea and Bacteriamentioning

confidence: 99%

Early Evolution of Transcription Systems and Divergence of Archaea and Bacteria

Lei

Burton

2021

Front. Mol. Biosci.

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DNA template-dependent multi-subunit RNA polymerases (RNAPs) found in all three domains of life and some viruses are of the two-double-Ψ-β-barrel (DPBB) type. The 2-DPBB protein format is also found in some RNA template-dependent RNAPs and a major replicative DNA template-dependent DNA polymerase (DNAP) from Archaea (PolD). The 2−DPBB family of RNAPs and DNAPs probably evolved prior to the last universal common cellular ancestor (LUCA). Archaeal Transcription Factor B (TFB) and bacterial σ factors include homologous strings of helix-turn-helix units. The consequences of TFB-σ homology are discussed in terms of the evolution of archaeal and bacterial core promoters. Domain-specific DPBB loop inserts functionally connect general transcription factors to the RNAP active site. Archaea appear to be more similar to LUCA than Bacteria. Evolution of bacterial σ factors from TFB appears to have driven divergence of Bacteria from Archaea, splitting the prokaryotic domains.

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“…Lane and Martin claim that eukaryotes have, on average, ~200,000 times more 'energy per gene' than prokaryotes (3). Such a drastic energetic difference is supposedly caused by two major advantages conferred by mitochondria upon eukaryotes (3,(16)(17)(18). The first one is the internalization and expansion of respiratory membranes within mitochondria which released eukaryotes of surface-area constraints.…”

Section: Introductionmentioning

confidence: 99%

The role of mitochondrial energetics in the origin and diversification of eukaryotes

Schavemaker

Muñoz-Gómez

2021

Preprint

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The origin of eukaryotic cell size and complexity is thought by some to have required an energy excess provided by mitochondria, whereas others claim that mitochondria provide no energetic boost to eukaryotes. Recent observations show that energy demand scales continuously and linearly with cell volume across both prokaryotes and eukaryotes, and thus suggest that eukaryotes do not have an increased energetic capacity over prokaryotes. However, amounts of respiratory membranes and ATP synthases scale super-linearly with cell surface area. Furthermore, the energetic consequences of the contrasting genomic designs between prokaryotes and eukaryotes have yet to be precisely quantified. Here, we investigated (1) potential factors that affect the cell volumes at which prokaryotes become surface area-constrained, and (2) the amount of energy that is divested to increasing amounts of DNA due to the contrasting genomic designs of prokaryotes and eukaryotes. Our analyses suggest that prokaryotes are not necessarily constrained by their cell surfaces at cell volumes of 100-103 µm3, and that the genomic design of eukaryotes is only slightly advantageous at genomes sizes of 106-107 bp. This suggests that eukaryotes may have first evolved without the need for mitochondria as these ranges hypothetically encompass the Last Eukaryote Common Ancestor and its proto-eukaryotic ancestors. However, our analyses also show that increasingly larger and fast-dividing prokaryotes would have a shortage of surface area devoted to respiration and would disproportionally divest more energy to DNA synthesis at larger genome sizes. We thus argue that, even though mitochondria may not have been required by the first eukaryotes, the successful diversification of eukaryotes into larger and more active cells was ultimately contingent upon the origin of mitochondria.

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How energy flow shapes cell evolution

Abstract: Evolution of enzymatic activities in the orotidine 5'-monophosphate decarboxylase suprafamily: structural basis for catalytic promiscuity in wild-type and designed mutants of 3-keto-L-gulonate 6-phosphate decarboxylase.

Cited by 34 publications

References 42 publications

Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Early Evolution of Transcription Systems and Divergence of Archaea and Bacteria

The role of mitochondrial energetics in the origin and diversification of eukaryotes

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