Evolutionary origins and specialisation of membrane transport

Dacks, Joel B.; Field, Mark C.

doi:10.1016/j.ceb.2018.06.001

Cited by 51 publications

(51 citation statements)

References 57 publications

(73 reference statements)

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“…These all constitute areas of biological function that were greatly modified as nuclear material was moved into the nucleus, the processes of transcription and translation were isolated and localised to specific regions within the cell forcing the machinery for them to be moved into the correct organelle and the products of these processes transported correctly 13,72 . As processes became specialised and sub-localised in their own organelles and vesicles, the categories of pathways affected are entirely in-line with those that needed to have become heavily modified 14,44 . Accordingly the functional annotations of the genes involved show a large propensity to be involved in Membrane Trafficking, various aspects of Genetic Information Processing, and signal transduction, consistent with establishing a system of intracellular biology of sub-compartmentalised processes and the regulatory systems for controlling them.…”

Section: Discussionmentioning

confidence: 89%

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Newman

Moore

et al. 2019

Preprint

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It is still a matter of debate whether the First Eukaryote Common Ancestor (FECA) arose from the merger of an archaeal host with an alphaproteobacterium, or was a proto-eukaryote with significant eukaryotic characteristics way before endosymbiosis occurred. The Last Eukaryote Common Ancestor (LECA) as its descendant is thought to be an entity that possessed functional and cellular complexity comparable to modern organisms. The precise nature and physiology of both of these organisms has been a long-standing, unanswered question in evolutionary and cell biology. Recently, a much broader diversity of eukaryotic genomes has become available and this means we can reconstruct early eukaryote evolution with a greater deal of precision. Here, we reconstruct a hypothetical genome for LECA from modern eukaryote genomes. The constituent genes were mapped onto 454 pathways from the KEGG database covering cellular, genetic, and metabolic processes across six model species to provide functional insights into it's capabilities. We reconstruct a LECA that was a facultatively anaerobic, single-celled organism, similar to a modern Protist possessing complex predatory and sexual behaviour. We go on to examine how much of these capabilities arose along the FECA-to-LECA transition period. We see a at least 1,554 genes gained by FECA during this evolutionary period with extensive remodelling of pathways relating to lipid metabolism, cellular processes, genetic information processing, protein processing, and signalling. We extracted the BRITE classifications for the genes from the KEGG database, which arose during the transition from FECA-to-LECA and examine the types of genes that saw the most gains and what novel classifications were introduced. Two-thirds of our reconstructed LECA genome appears to be prokaryote in origin and the remaining third consists of genes with functional classifications that originate from prokaryote homologs in our LECA genome. Signal transduction and Post Translational Modification elements stand out as the primary novel classes of genes developed during this period. These results suggest that largely the eukaryote common ancestors achieved the defining characteristics of modern eukaryotes by primarily expanding on prokaryote biology and gene families.

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Section: Discussionmentioning

confidence: 89%

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Newman

Moore

et al. 2019

Preprint

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“…Previous work demonstrated that gene duplications nearly doubled the genome 4 . Gene families such as small GTPases, kinesins and vesicle coat proteins greatly expanded, which enabled proto-eukaryotes to employ an elaborate intracellular signalling network, a vesicular trafficking system and a dynamic cytoskeleton [13][14][15][16] . Uncovering the order in which these and other eukaryotic features emerged is complicated due to the absence of intermediate life forms.…”

Section: Main Textmentioning

confidence: 99%

Timing the origin of eukaryotic cellular complexity with ancient duplications

Vosseberg

Hooff

Marcet‐Houben

et al. 2019

Preprint

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Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells 1,2 . The last eukaryotic common ancestor (LECA) harboured intracellular compartments, including mitochondria. In addition to mitochondrial endosymbiosis, eukaryogenesis was driven by numerous gene acquisitions 3 , inventions and duplications 4 , which shaped the ancestral eukaryotic traits. While evolutionary intermediates are lacking, gene duplications allow us to elucidate the order of events by which eukaryotes originated. Here we reconstruct successive steps during eukaryogenesis using phylogenomics and show that mitochondrial endosymbiosis was an intermediate episode. We found that gene duplications roughly doubled the proto-eukaryotic genome, with families inherited from the Asgard archaea-related host being duplicated most. Importantly, by relatively timing events using branch lengths we inferred that duplications of archaeal families occurred throughout eukaryogenesis, both before and after the acquisition of bacterial genes. Duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded primarily after mitochondrial endosymbiosis. Altogether, we demonstrate that the host that engulfed the protomitochondrion had some eukaryote-like complexity, which further increased drastically upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes 5,6 to the proposed role of mitochondria in triggering eukaryogenesis 7,8 .

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“…The different organelles of the endocytic and secretory pathways are populated with membrane proteins that confer a specific function and identity to the various organelles and therefore the mechanisms that control the movement and exchange of membrane proteins between the different organelles need to be highly sophisticated and efficient to ensure the correct membrane protein is delivered to the appropriate organelle. This process is known as membrane trafficking and the mechanisms and principles of membrane trafficking are generally very well conserved through evolution (for review see [1] ) -see Figure 1.…”

Section: Introductionmentioning

confidence: 99%

Back From the Brink: Retrieval of Membrane Proteins From Terminal Compartments

Seaman

2019

BioEssays

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Contact : mnjs100@cam.ac.uk, 44-1223-763225. SubtitleUnexpected pathways for membrane protein retrieval from vacuoles and endolysosomes. SummaryIt has long been believed that membrane proteins present in degradative compartments such as endolysosomes or vacuoles would be destined for destruction. Now however, it appears that mechanisms and machinery exist in simple eukaryotes such as yeast and more complex organisms such as mammals that can rescue potentially 'doomed' membrane proteins by retrieving them from these 'late' compartments and recycling them back to the Golgi complex. In yeast, a sorting nexin dimer containing Snx4p can recognise and retrieve the Atg27p membrane protein whilst in mammals, the AP5 complex (with SPG11 and SPG15) directs the recycling of Golgi-localised proteins along with the cation-independent mannose 6-phosphate receptor (CIMPR). Although the respective machinery is different, there is much commonality between yeast and mammals regarding the mechanisms of retrieval and the physiological importance of these late recycling pathways.

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Evolutionary origins and specialisation of membrane transport

Cited by 51 publications

References 57 publications

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Timing the origin of eukaryotic cellular complexity with ancient duplications

Back From the Brink: Retrieval of Membrane Proteins From Terminal Compartments

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