Comparative Analysis of Bacillariophyceae Chloroplast Genomes Uncovers Extensive Genome Rearrangements Associated with Speciation

Abstract

The Bacillariophyceae is a species-rich, ecologically significant class of Bacillariophyta. Despite their critical importance in marine ecosystems as primary producers and in the development of harmful algal blooms (HABs), taxonomic research on Bacillariophyceae species has been hindered because of their limited morphological features, plasticity of morphologies, and the low resolution of common molecular markers. Hence molecular markers with improved resolution are urgently needed. Organelle genomes, which can be constructed efficiently with the recent development of high throughput DNA sequencing technologies and the advancement of bioinformatics tools, have been proposed as super barcodes for their higher resolution for distinguishing different species and intra-species genomic variations. In this study, we tested the value of full-length chloroplast genomes (cpDNAs) as super barcodes for distinguishing diatom species, by constructing cpDNAs of 11 strains of the class Bacillariophyceae, including Nitzschia ovalis, Nitzschia traheaformis, Cylindrotheca spp., Psammodictyon constrictum, Bacillaria paxillifer, two strains of Haslea tsukamotoi, Haslea avium, Navicula arenaria, and Pleurosigma sp. Comparative analysis of cpDNAs revealed that cpDNAs were not only adequate for resolving different species, but also for enabling recognition of high levels of genome rearrangements between cpDNAs of different species, especially for species of the genera Nitzschia, Cylindrotheca, Navicula and Haslea. Additionally, comparative analysis suggested that the positioning of species in the genus Haslea should be transferred to the genus Navicula. Chloroplast genome-based evolutionary analysis suggested that the Bacillariophyceae species first appeared during the Cretaceous period and the diversity of species rose after the mass extinction about 65 Mya. This study highlighted the value of cpDNAs in research on the biodiversity and evolution of Bacillariophyceae species, and, with the construction of more cpDNAs representing additional genera, deeper insight into the biodiversity and evolutionary relationships of Bacillariophyceae species will be gained.