Comparative Genomics for Evolutionary Cell Biology Using AMOEBAE: Understanding the Golgi and Beyond

Barlow, Lael D.; Maciejowski, William; More, Kiran; Terry, Kara; Vargová, Romana; Záhonová, Kristína; Dacks, Joel B.

doi:10.1007/978-1-0716-2639-9_26

Cited by 10 publications

(7 citation statements)

References 54 publications

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“…Hits were considered positive if the reverse search yielded the human protein within three iterations, and had at least two orders of magnitude e-value difference between the next non-redundant hit. BLAST and HMMER results were performed and parsed using the AMOEBAE workflow using a maximum e-value of 0.05 and a minimum difference in e-value order of magnitude of 2 (Barlow et al, 2023), while JackHMMER results were parsed using in-house scripts (available on Figshare). Phylogenies were used to confirm identities between known paralogs (HPS1/MON1, HPS4/CCZ1, and HPS5/TECPR2).…”

Section: Methodsmentioning

confidence: 99%

The evolutionary origins of the lysosome-related organelle sorting machinery reveal fundamental homology in post-endosome trafficking pathways

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Dacks,

Manna

2024

Preprint

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The major organelles and pathways of the endomembrane system were in place by the time of the last eukaryotic common ancestor (LECA) (~1.5 billion years ago) and their acquisition were defining milestones during the process of eukaryogenesis itself. Comparative cell biology and evolutionary analyses show multiple instances of homology in the protein machinery controlling distinct inter-organelle trafficking routes. Resolving these homologous relationships allows us to explore processes underlying the emergence of new cellular compartments, infer ancestral states pre-dating LECA, and can even provide insight into the process of eukaryogenesis itself. Here we undertake a molecular evolutionary analysis, including providing a transcriptome of the jakobid flagellate Reclinomonas americana, exploring the origins of the machinery responsible for the biogenesis of lysosome-related organelles, the so-called Biogenesis of Lysosome-related Organelle Complexes (BLOCs 1,2, and 3). This pathway has been studied only in animals and is not considered a feature of the basic eukaryotic cell plan. We show that this machinery, and by inference the corresponding sorting pathway, was likely in place prior to the divergence of eukaryotes and is found in a much more diverse array of eukaryotes than is currently assumed. As such, this sorting pathway is likely an underappreciated facet of broader eukaryotic cellular function. Moreover, we resolve multiple points of ancient homology between all three BLOCs and other post-endosomal retrograde trafficking machinery (BORC, CCZ1/MON1, and a newly identified relationship with HOPS/CORVET) offering a mechanistic and evolutionary unification of these trafficking pathways. Overall, this study provides a comprehensive account of the rise of the LRO biogenesis machinery from prokaryotic origins to current eukaryotic diversity, Asgard archaea to animals, integrating it into the larger mechanistic framework describing endomembrane evolution.

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Section: Methodsmentioning

confidence: 99%

The evolutionary origins of the lysosome-related organelle sorting machinery reveal fundamental homology in post-endosome trafficking pathways

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Dacks,

Manna

2024

Preprint

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“…If the best hit was the protein of interest and had an E-value two orders of magnitude lower than the next non-orthologous hit, this was considered as orthology validation. Forward and reverse searches were performed using the AMOEBAE tool 48 .…”

Section: Methodsmentioning

confidence: 99%

High quality genome and transcriptome data for two new species ofMantamonas, a deep-branching eukaryote clade

Blaz

Galindo

Heiss

et al. 2023

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Mantamonads were long considered to represent an "orphan" lineage in the tree of eukaryotes, likely branching near the most frequently assumed position for the root of eukaryotes. Recent phylogenomic analyses have placed them as part of the "CRuMs" supergroup, along with collodictyonids and rigifilids. This supergroup appears to branch at the base of Amorphea, making it of special importance for understanding the deep evolutionary history of eukaryotes. However, the lack of representative species and complete genomic data associated with them has hampered the investigation of their biology and evolution. Here, we isolated and described two new species of mantamonads, Mantamonas vickermani sp. nov. and Mantamonas sphyraenae sp. nov., for each of which we generated transcriptomic sequence data, as well as a high-quality genome for the latter. The estimated size of the M. sphyraenae genome is 25 Mb; our de novo assembly appears to be highly contiguous and complete with 9,416 predicted protein-coding genes. This near-chromosome-scale genome assembly is the first described for the CRuMs supergroup.

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“…Homology searches of the components in Endomembrane Retrograde transport machineries and their cargoes were conducted using A nalysis of Mo lecular E volution with BA tch E ntry (AMOEBAE) (Barlow et al, 2023). Homo sapiens and Saccharomyces cerevisiae protein sequences from NCBI were used as queries for the initial homology searches.…”

Section: Experiments Proceduresmentioning

confidence: 99%

Tracing back the expansion of the endomembrane rescue systems in parasitic Parabasalids to the ancestral origin in its free-living sister lineage

Shinde,

Kucerova,

Dacks

et al. 2024

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Early Endosomes sort transmembrane cargo whether for lysosomal degradation or retrieval to the plasma membrane or the Golgi complex. Endosomal retrieval in eukaryotes is governed by the anciently homologous Retromer or Retriever complexes. Each comprises a core tri-protein subcomplex, membrane-deformation proteins, and interacting partner complexes, together retrieving a variety of known cargo proteins. Trichomonas vaginalis; a sexually transmitted human parasite uses the endomembrane system for pathogenesis. It has massively and selectively expanded its endomembrane protein complement, the evolutionary path of which has been largely unexplored. Our molecular evolutionary study of Retromer, Retriever and associated machinery in parabasalids and its free-living sister lineage of Anaeramoeba, demonstrates specific expansion of the Retromer machinery, contrasting with the Retriever components. We also observe partial loss of Commander complex and Sorting Nexins in Parabasalia but complete retention in Anaeramoeba. Notably, we identify putative parabasalid Sorting Nexin analogues. Finally, we report the first Retriever protein localization in a non- metazoan group along with Retromer protein localization in T. vaginalis. Therefore, we provide a unique genome expansion study of endomembrane trafficking system in parasitic and free- living protists alike.

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Comparative Genomics for Evolutionary Cell Biology Using AMOEBAE: Understanding the Golgi and Beyond

Cited by 10 publications

References 54 publications

The evolutionary origins of the lysosome-related organelle sorting machinery reveal fundamental homology in post-endosome trafficking pathways

The evolutionary origins of the lysosome-related organelle sorting machinery reveal fundamental homology in post-endosome trafficking pathways

High quality genome and transcriptome data for two new species ofMantamonas, a deep-branching eukaryote clade

Tracing back the expansion of the endomembrane rescue systems in parasitic Parabasalids to the ancestral origin in its free-living sister lineage

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