The complete maternally and paternally inherited mitochondrial genomes of the endangered freshwater mussel Solenaia carinatus (Bivalvia: Unionidae) and implications for Unionidae taxonomy.

Jun Rong,Yuan Wan,Chun-Hua Zhou,Ming-Hua Zhang,Xiao-Chen Huang,Shan Ouyang,Xiao-Ping Wu,Yong Liu

doi:10.1371/journal.pone.0084352

Abstract

Doubly uniparental inheritance (DUI) is an exception to the typical maternal inheritance of mitochondrial (mt) DNA in Metazoa, and found only in some bivalves. In species with DUI, there are two highly divergent gender-associated mt genomes: maternal (F) and paternal (M), which transmit independently and show different tissue localization. Solenaia carinatus is an endangered freshwater mussel species exclusive to Poyang Lake basin, China. Anthropogenic events in the watershed greatly threaten the survival of this species. Nevertheless, the taxonomy of S. carinatus based on shell morphology is confusing, and the subfamilial placement of the genus Solenaia remains unclear. In order to clarify the taxonomic status and discuss the phylogenetic implications of family Unionidae, the entire F and M mt genomes of S. carinatus were sequenced and compared with the mt genomes of diverse freshwater mussel species. The complete F and M mt genomes of S. carinatus are 16716 bp and 17102 bp in size, respectively. The F and M mt genomes of S. carinatus diverge by about 40% in nucleotide sequence and 48% in amino acid sequence. Compared to F counterparts, the M genome shows a more compact structure. Different gene arrangements are found in these two gender-associated mt genomes. Among these, the F genome cox2-rrnS gene order is considered to be a genome-level synapomorphy for female lineage of the subfamily Gonideinae. From maternal and paternal mtDNA perspectives, the phylogenetic analyses of Unionoida indicate that S. carinatus belongs to Gonideinae. The F and M clades in freshwater mussels are reciprocal monophyly. The phylogenetic trees advocate the classification of sampled Unionidae species into four subfamilies: Gonideinae, Ambleminae, Anodontinae, and Unioninae, which is supported by the morphological characteristics of glochidia.

Highlights

Unionoid bivalves, known as freshwater mussels (Bivalvia: Unionoida), are one of the most important faunas in freshwater ecosystems, for their potentials to enhance biodiversity and ecosystem functioning (e.g., 1,2)
We described the first complete maternally and paternally inherited mitochondrial genomes of S. carinatus, and inferred the phylogenetic trees together with the published mitogenome data of unionoids, expecting the classification of unionids could reflect natural relationships with robust molecular evidence
The handling of mussels was conducted in accordance with the guidelines on the care and use of animals for scientific purposes set by the Institutional Animal Care and Use Committee (IACUC) of Nanchang University, Jiangxi, China

Summary

Introduction

Known as freshwater mussels (Bivalvia: Unionoida), are one of the most important faunas in freshwater ecosystems, for their potentials to enhance biodiversity and ecosystem functioning (e.g., 1,2). The family Unionidae is the most species-rich of the Unionoida and broadly distributed across North America and Eurasia as well as tropical Mesoamerica, Africa, and southeastern Asia [3]. Freshwater mussels have a distinct parasitic stage in the life cycle that involves a host-fish and a highly modified larva, the glochidium [6]. They are sensitive to environmental changes, especially in the post-parasitic phase [7,8,9]. More than 80% of the unionid species in these regions are considered to be threatened or near threatened, and the dominant taxa of bivalves have shifted from large-sized unionids to the smallsized clams [12]

Methods

Results

Conclusion