Dataset Information

Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era.

ABSTRACT:

Background

The last eukaryotic common ancestor already had an amazingly complex cell possessing genomic and cellular features such as spliceosomal introns, mitochondria, cilia-dependent motility, and a cytoskeleton together with several intracellular transport systems. In contrast to the microtubule-based dyneins and kinesins, the actin-filament associated myosins are considerably divergent in extant eukaryotes and a unifying picture of their evolution has not yet emerged.

Results

Here, we manually assembled and annotated 7852 myosins from 929 eukaryotes providing an unprecedented dense sequence and taxonomic sampling. For classification we complemented phylogenetic analyses with gene structure comparisons resulting in 79 distinct myosin classes. The intron pattern analysis and the taxonomic distribution of the classes suggest two myosins in the last eukaryotic common ancestor, a class-1 prototype and another myosin, which is most likely the ancestor of all other myosin classes. The sparse distribution of class-2 and class-4 myosins outside their major lineages contradicts their presence in the last eukaryotic common ancestor but instead strongly suggests early eukaryote-eukaryote horizontal gene transfer.

Conclusions

By correlating the evolution of myosin diversity with the history of Earth we found that myosin innovation occurred in independent major "burst" events in the major eukaryotic lineages. Most myosin inventions happened in the Mesoproterozoic era. In the late Neoproterozoic era, a process of extensive independent myosin loss began simultaneously with further eukaryotic diversification. Since the Cambrian explosion, myosin repertoire expansion is driven by lineage- and species-specific gene and genome duplications leading to subfunctionalization and fine-tuning of myosin functions.

SUBMITTER: Kollmar M

PROVIDER: S-EPMC5583752 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era.

Kollmar Martin M Mühlhausen Stefanie S

BMC evolutionary biology 20170904 1

<h4>Background</h4>The last eukaryotic common ancestor already had an amazingly complex cell possessing genomic and cellular features such as spliceosomal introns, mitochondria, cilia-dependent motility, and a cytoskeleton together with several intracellular transport systems. In contrast to the microtubule-based dyneins and kinesins, the actin-filament associated myosins are considerably divergent in extant eukaryotes and a unifying picture of their evolution has not yet emerged.<h4>Results</h4 ...[more]

PMID: 28870165

Similar Datasets

Project description:Marrow adipose tissue (MAT) is an endocrine organ with the potential to influence skeletal remodeling and hematopoiesis. Pathologic MAT expansion has been studied in the context of severe metabolic challenge, including caloric restriction, high fat diet feeding, and leptin deficiency. However, the rapid change in peripheral fat and glucose metabolism associated with these models impedes our ability to examine which metabolic parameters precede or coincide with MAT expansion. Microfibril-associated glycoprotein-1 (MAGP1) is a matricellular protein that influences cellular processes by tethering signaling molecules to extracellular matrix structures. MAGP1-deficient (Mfap2 (-/-)) mice display a progressive excess adiposity phenotype, which precedes insulin resistance and occurs without changes in caloric intake or ambulation. Mfap2 (-/-) mice were, therefore, used as a model to associate parameters of metabolic disease, bone remodeling, and hematopoiesis with MAT expansion. Marrow adiposity was normal in Mfap2 (-/-) mice until 6?months of age; however, by 10?months, marrow fat volume had increased fivefold relative to wild-type control at the same age. Increased gonadal fat pad mass and hyperglycemia were detectable in Mfap2 (-/-) mice by 2?months, but peaked by 6?months. The development of insulin resistance coincided with MAT expansion. Longitudinal characterization of bone mass demonstrated a disconnection in MAT volume and bone volume. Specifically, Mfap2 (-/-) mice had reduced trabecular bone volume by 2?months, but this phenotype did not progress with age or MAT expansion. Interestingly, MAT expansion in the 10-month-old Mfap2 (-/-) mice was associated with modest alterations in basal hematopoiesis, including a shift from granulopoiesis to B lymphopoiesis. Together, these findings indicate MAT expansion is coincident with insulin resistance, but not excess peripheral adiposity or hyperglycemia in Mfap2 (-/-) mice; and substantial MAT accumulation does not necessitate a proportional decrease in either bone mass or bone marrow cellularity.

Project description:BACKGROUND: Yeast and animal cells require six mini-chromosome maintenance proteins (Mcm2-7) for pre-replication complex formation, DNA replication initiation and DNA synthesis. These six individual MCM proteins form distinct heterogeneous subunits within a hexamer which is believed to form the replicative helicase and which associates with the essential but non-homologous Mcm10 protein during DNA replication. In contrast Archaea generally only possess one MCM homologue which forms a homohexameric MCM helicase. In some eukaryotes Mcm8 and Mcm9 paralogues also appear to be involved in DNA replication although their exact roles are unclear. RESULTS: We used comparative genomics and phylogenetics to reconstruct the diversification of the eukaryotic Mcm2-9 gene family, demonstrating that Mcm2-9 were formed by seven gene duplication events before the last common ancestor of the eukaryotes. Mcm2-7 protein paralogues were present in all eukaryote genomes studied suggesting that no gene loss or functional replacements have been tolerated during the evolutionary diversification of eukaryotes. Mcm8 and 9 are widely distributed in eukaryotes and group together on the MCM phylogenetic tree to the exclusion of all other MCM paralogues suggesting co-ancestry. Mcm8 and Mcm9 are absent in some taxa, including Trichomonas and Giardia, and appear to have been secondarily lost in some fungi and some animals. The presence and absence of Mcm8 and 9 is concordant in all taxa sampled with the exception of Drosophila species. Mcm10 is present in most eukaryotes sampled but shows no concordant pattern of presence or absence with Mcm8 or 9. CONCLUSION: A multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes. The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions. Mcm8 and 9 evolved early in eukaryote cell evolution and their pattern of presence or absence suggests that they may have linked functions. Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.

Dataset Information

Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era.

Background

Results

Conclusions

Publications

Myosin repertoire expansion coincides with eukaryotic diversification in the Mesoproterozoic era.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets