A proposed method for analyzing molecular signatures to detect hermaphroditism in freshwater mussels: a case study using the Eastern Floater (Pyganodon cataracta)

2021 ◽  
Author(s):  
Donald T. Stewart ◽  
Chloe M. Stephenson ◽  
Ljiljana M. Stanton ◽  
Emily E. Chase ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Freshwater Mussels ◽  
Uniparental Inheritance ◽  
Molecular Signatures ◽  
Doubly Uniparental Inheritance ◽  
Hydrophobic Properties ◽  
Mt Dna ◽  
Reading Frame ◽  
Mt Genome ◽  
Primary Nucleotide Sequence

Many freshwater mussels (Order Unionida) have an unusual system of doubly uniparental inheritance (DUI) of mitochondrial (mt) DNA. In species with DUI, males possess a female-transmitted (F-type) mt genome and a male-transmitted (M-type) mt genome. These genomes contain non-canonical open reading frame (orf) genes referred to as f-orf and m-orf, present in F and M mt genomes, respectively. These genes have been implicated in sexual development in Unionida. When gonochoric species become hermaphroditic, which has happened several times in Unionida, they lose their M-type mt genome, and f-orf genes evolve dramatically. Resulting F-ORF proteins are highly divergent in terms of primary nucleotide sequence, inferred amino acids, and hydrophobic properties; these genes (and proteins) are referred to as hermaphroditic orfs or h-orfs (and H-ORFs). We investigated patterns of hydrophobicity divergence for H-ORF proteins in hermaphrodites versus F-ORF proteins in closely related gonochoric species against cytochrome c oxidase subunit 1 (cox1) divergences. This approach was used to assess whether cryptic hermaphrodites can be detected. Although we did not detect evidence for the recent transition of any populations of Eastern Floaters, Pyganodon cataracta (Say, 1817) to hermaphroditism, our analyses demonstrate that molecular signatures in mtDNA can be used to detect hermaphroditism in freshwater mussels.

scholarly journals Genome survey of the freshwater mussel Venustaconcha ellipsiformis (Bivalvia: Unionida) using a hybrid de novo assembly approach

2018 ◽  
Author(s):  
Sébastien Renaut ◽  
Davide Guerra ◽  
Walter R. Hoeh ◽  
Donald T. Stewart ◽  
Arthur E. Bogan ◽  
...  
Keyword(s):  
De Novo ◽  
Freshwater Mussels ◽  
Draft Genome ◽  
Uniparental Inheritance ◽  
Ecological Value ◽  
Doubly Uniparental Inheritance ◽  
Total Size ◽  
High Coverage ◽  
Genome Coverage ◽  
Eukaryotic Genes

AbstractFreshwater mussels (Bivalvia: Unionida) serve an important role as aquatic ecosystem engineers but are one of the most critically imperilled groups of animals. Here, we used a combination of sequencing strategies to assemble and annotate a draft genome of Venustaconcha ellipsiformis, which will serve as a valuable genomic resource given the ecological value and unique “doubly uniparental inheritance” mode of mitochondrial DNA transmission of freshwater mussels. The genome described here was obtained by combining high coverage short reads (65X genome coverage of Illumina paired-end and 11X genome coverage of mate-pairs sequences) with low coverage Pacific Biosciences long reads (0.3X genome coverage). Briefly, the final scaffold assembly accounted for a total size of 1.54Gb (366,926 scaffolds, N50 = 6.5Kb, with 2.3% of “N” nucleotides), representing 86% of the predicted genome size of 1.80Gb, while over one third of the genome (37.5%) consisted of repeated elements and more than 85% of the core eukaryotic genes were recovered. Given the repeated genetic bottlenecks of V. ellipsiformis populations as a result of glaciations events, heterozygosity was also found to be remarkably low (0.6%), in contrast to most other sequenced bivalve species. Finally, we reassembled the full mitochondrial genome and found six polymorphic sites with respect to the previously published reference. This resource opens the way to comparative genomics studies to identify genes related to the unique adaptations of freshwater mussels and their distinctive mitochondrial inheritance mechanism.

scholarly journals Evaluating the utility of the female-specific mitochondrialf-orfgene for population genetic, phylogeographic and systematic studies in freshwater mussels (Bivalvia: Unionida)

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5007 ◽  
Author(s):  
Brent M. Robicheau ◽  
Emily E. Chase ◽  
Walter R. Hoeh ◽  
John L. Harris ◽  
Donald T. Stewart ◽  
...  
Keyword(s):  
Population Genetic ◽  
Freshwater Mussels ◽  
Mitochondrial Protein ◽  
Species Level ◽  
Uniparental Inheritance ◽  
Genome Sequences ◽  
Doubly Uniparental Inheritance ◽  
Protein Coding ◽  
Coding Regions ◽  
Female Specific

Freshwater mussels (order: Unionida) represent one of the most critically imperilled groups of animals; consequently, there exists a need to establish a variety of molecular markers for population genetics and systematic studies in this group. Recently, two novel mitochondrial protein-coding genes were described in unionoids with doubly uniparental inheritance of mtDNA. These genes are thef-orfin female-transmitted mtDNA and them-orfin male-transmitted mtDNA. In this study, whole F-type mitochondrial genome sequences of two morphologically similarLampsilisspp. were compared to identify the most divergent protein-coding regions, including thef-orfgene, and evaluate its utility for population genetic and phylogeographic studies in the subfamily Ambleminae. We also tested whether thef-orfgene is phylogenetically informative at the species level. Our preliminary results indicated that thef-orfgene could represent a viable molecular marker for population- and species-level studies in freshwater mussels.

scholarly journals Distribution and frequency of mitochondrial DNA polymorphisms in blue mussel (Mytilus edulis) populations of southwestern Nova Scotia (Canada)

2018 ◽  
Vol 96 (6) ◽  
pp. 608-613 ◽  
Author(s):  
Donald T. Stewart ◽  
Marion Sinclair-Waters ◽  
Alexandra Rice ◽  
Ryan A. Bunker ◽  
Brent M. Robicheau ◽  
...  
Keyword(s):  
Nova Scotia ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Phylogenetic Analyses ◽  
Role Reversal ◽  
Dna Polymorphisms ◽  
Swimming Velocity ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Mt Genome

The Atlantic blue mussel (Mytilus edulis Linnaeus, 1758) exhibits doubly uniparental inheritance of mitochondrial (mt) DNA. Females are usually homoplasmic for a female-transmitted mt genome (the F type) and males are heteroplasmic for an F type and a male-transmitted mt genome (the M type). F types can undergo “role-reversal” events, resulting in new male-transmitted mtDNA genomes known as recently masculinized (RM) types that co-occur in populations with evolutionarily older standard-male (SM) types. Phylogenetic analyses have shown that RM types periodically replace SM types. It has also been shown that sperm with RM mtDNA have greater swimming velocity and more efficient components of the electron transport chain compared to sperm with SM mtDNA, thus leading to the hypothesis that RM sperm may have a selective advantage over SM sperm. The present study examines the distribution of RM and SM mitotypes in male M. edulis (n = 225) from 13 localities in southwestern Nova Scotia (Canada). The SM type was more common in all populations, with the proportion of RM types ranging from 0% to 24.1%. The highest proportion of RM types was observed in an aquaculture operation. Analyses of additional populations are required to evaluate the selective pressures affecting the geographic distribution of RM and SM mitotypes in M. edulis.

scholarly journals Variability of mitochondrial ORFans hints at possible differences in the system of doubly uniparental inheritance of mitochondria among families of freshwater mussels (Bivalvia: Unionida)

2019 ◽  
Vol 19 (1) ◽  
Author(s):  
Davide Guerra ◽  
Manuel Lopes-Lima ◽  
Elsa Froufe ◽  
Han Ming Gan ◽  
Paz Ondina ◽  
...  
Keyword(s):  
Freshwater Mussels ◽  
Complete Mitochondrial Genome ◽  
Physiological Role ◽  
Freshwater Mussel ◽  
Single Species ◽  
Open Reading Frames ◽  
Uniparental Inheritance ◽  
Doubly Uniparental Inheritance ◽  
Sexual Systems ◽  
Mitogenome Sequence

Abstract Background Supernumerary ORFan genes (i.e., open reading frames without obvious homology to other genes) are present in the mitochondrial genomes of gonochoric freshwater mussels (Bivalvia: Unionida) showing doubly uniparental inheritance (DUI) of mitochondria. DUI is a system in which distinct female-transmitted and male-transmitted mitotypes coexist in a single species. In families Unionidae and Margaritiferidae, the transition from dioecy to hermaphroditism and the loss of DUI appear to be linked, and this event seems to affect the integrity of the ORFan genes. These observations led to the hypothesis that the ORFans have a role in DUI and/or sex determination. Complete mitochondrial genome sequences are however scarce for most families of freshwater mussels, therefore hindering a clear localization of DUI in the various lineages and a comprehensive understanding of the influence of the ORFans on DUI and sexual systems. Therefore, we sequenced and characterized eleven new mitogenomes from poorly sampled freshwater mussel families to gather information on the evolution and variability of the ORFan genes and their protein products. Results We obtained ten complete plus one almost complete mitogenome sequence from ten representative species (gonochoric and hermaphroditic) of families Margaritiferidae, Hyriidae, Mulleriidae, and Iridinidae. ORFan genes are present only in DUI species from Margaritiferidae and Hyriidae, while non-DUI species from Hyriidae, Iridinidae, and Mulleriidae lack them completely, independently of their sexual system. Comparisons among the proteins translated from the newly characterized ORFans and already known ones provide evidence of conserved structures, as well as family-specific features. Conclusions The ORFan proteins show a comparable organization of secondary structures among different families of freshwater mussels, which supports a conserved physiological role, but also have distinctive family-specific features. Given this latter observation and the fact that the ORFans can be either highly mutated or completely absent in species that secondarily lost DUI depending on their respective family, we hypothesize that some aspects of the connection among ORFans, sexual systems, and DUI may differ in the various lineages of unionids.

scholarly journals Mitogenomics of Perumytilus purpuratus (Bivalvia: Mytilidae) and its implications for doubly uniparental inheritance of mitochondria

PeerJ ◽  
2018 ◽  
Vol 6 ◽  
pp. e5593 ◽  
Author(s):  
Beata Śmietanka ◽  
Marek Lubośny ◽  
Aleksandra Przyłucka ◽  
Karin Gérard ◽  
Artur Burzyński
Keyword(s):  
Purifying Selection ◽  
Mitochondrial Genomes ◽  
Uniparental Inheritance ◽  
Maternal Lineage ◽  
Doubly Uniparental Inheritance ◽  
Reading Frame ◽  
Musculista Senhousia ◽  
Perumytilus Purpuratus ◽  
First Time ◽  
Complete Mitochondrial Genomes

Animal mitochondria are usually inherited through the maternal lineage. The exceptional system allowing fathers to transmit their mitochondria to the offspring exists in some bivalves. Its taxonomic spread is poorly understood and new mitogenomic data are needed to fill the gap. Here, we present for the first time the two divergent mitogenomes from Chilean mussel Perumytilus purpuratus. The existence of these sex-specific mitogenomes confirms that this species has the doubly uniparental inheritance (DUI) of mitochondria. The genetic distance between the two mitochondrial lineages in P. purpuratus is not only much bigger than in the Mytilus edulis species complex but also greater than the distance observed in Musculista senhousia, the only other DUI-positive member of the Mytilidae family for which both complete mitochondrial genomes were published to date. One additional, long ORF (open reading frame) is present exclusively in the maternal mitogenome of P. purpuratus. This ORF evolves under purifying selection, and will likely be a target for future DUI research.

scholarly journals Differential Segregation Patterns of Sperm Mitochondria in Embryos of the Blue Mussel (Mytilus edulis)

Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 883-894
Author(s):  
Liqin Cao ◽  
Ellen Kenchington ◽  
Eleftherios Zouros
Keyword(s):  
Mitochondrial Dna ◽  
Mytilus Edulis ◽  
Blue Mussel ◽  
Uniparental Inheritance ◽  
Male Gonad ◽  
Doubly Uniparental Inheritance ◽  
Organelle Genomes ◽  
Somatic Tissues ◽  
Tight Linkage ◽  
Mitotracker Green

Abstract In Mytilus, females carry predominantly maternal mitochondrial DNA (mtDNA) but males carry maternal mtDNA in their somatic tissues and paternal mtDNA in their gonads. This phenomenon, known as doubly uniparental inheritance (DUI) of mtDNA, presents a major departure from the uniparental transmission of organelle genomes. Eggs of Mytilus edulis from females that produce exclusively daughters and from females that produce mostly sons were fertilized with sperm stained with MitoTracker Green FM, allowing observation of sperm mitochondria in the embryo by epifluorescent and confocal microscopy. In embryos from females that produce only daughters, sperm mitochondria are randomly dispersed among blastomeres. In embryos from females that produce mostly sons, sperm mitochondria tend to aggregate and end up in one blastomere in the two- and four-cell stages. We postulate that the aggregate eventually ends up in the first germ cells, thus accounting for the presence of paternal mtDNA in the male gonad. This is the first evidence for different behaviors of sperm mitochondria in developing embryos that may explain the tight linkage between gender and inheritance of paternal mitochondrial DNA in species with DUI.

Acute endurance exercise stimulates circulating levels of mitochondrial derived peptides in humans

2021 ◽  
Author(s):  
Ferdinand von Walden ◽  
Rodrigo Fernandez-Gonzalo ◽  
Jessica Maria Norrbom ◽  
Eric B. Emanuelsson ◽  
Vandre C. Figueiredo ◽  
...  
Keyword(s):  
Gene Expression ◽  
Skeletal Muscle ◽  
Diabetes Type 2 ◽  
Knee Extension ◽  
12S Rrna ◽  
Mt Dna ◽  
Reading Frame ◽  
Muscle Gene Expression ◽  
Muscle Gene ◽  
Circulating Levels

Mitochondrial derived peptides (MDPs) humanin (HN) and mitochondrial open reading frame of the 12S rRNA-c (MOTS-c) are involved in cell survival, suppression of apoptosis and metabolism. Circulating levels of MDPs are altered in chronic diseases such as diabetes type 2 and chronic kidney disease. Whether acute resistance (RE) or endurance (EE) exercise modulates circulating levels of HN and MOTS-c in humans is unknown. Following familiarization, subjects were randomized to EE (n=10, 45 min cycling at 70% of estimated VO2max), RE (n=10, 4 sets x 7RM, leg press and knee extension), or control (CON, n=10). Skeletal muscle biopsies and blood samples were collected before and at 30 minutes and 3 hours following exercise. Plasma concentration of HN and MOTS-c, skeletal muscle MOTS-c as well as gene expression of exercise related genes were analyzed. Acute EE and RE promoted changes in skeletal muscle gene expression typically seen in response to each exercise modality (c-Myc, 45S pre-rRNA, PGC-1α-total and PGC-1α-ex1b). At rest, circulating levels of HN were positively correlated to MOTS-c levels and age. Plasma levels of MDPs were not correlated to fitness outcomes (VO2max, leg strength or muscle mitochondrial (mt) DNA copy number). Circulating levels of HN were significantly elevated by acute EE but not RE. MOTS-C levels showed a trend to increase after EE. These results indicate that plasma MDP levels are not related to fitness status but that acute EE increases circulating levels of MDPs, in particular HN.

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