Abstract
BackgroundMitochondrial introns intermit coding regions of genes and feature characteristic secondary structures and splicing mechanisms. In metazoans, mitochondrial introns have only been detected in sponges, cnidarians, placozoans and one annelid species. Within demosponges, group I and group II introns are present in six families. Based on different insertion sites within the cox1 gene and secondary structures, four types of group I and two types of group II introns are known, which can harbor up to three encoding homing endonuclease genes (HEG) of the LAGLIDADG family (group I) and/or reverse transcriptase (group II). However, only little is known about sponge intron mobility, transmission, and origin due to the lack of a comprehensive dataset. We analyzed the largest dataset on sponge mitochondrial group I introns to date: 95 specimens, from 11 different sponge genera which provided novel insights into the evolution of group I introns.ResultsFor the first time group I introns were detected in four genera of the sponge family Scleritodermidae (Scleritoderma, Microscleroderma, Aciculites, Setidium). We demonstrated that group I introns in sponges aggregate in the most conserved regions of cox1. We showed that co-occurrence of two introns in cox1 is unique among metazoans, but not uncommon in sponges. However, this combination always associates an active intron with a degenerating one. Earlier hypotheses of HGT were confirmed and for the first time VGT and secondary losses of introns conclusively demonstrated.ConclusionThis study validates the subclass Spirophorina (Tetractinellida) as an intron hotspot in sponges. Our analyses confirm that most sponge group I introns probably originated from fungi. DNA barcoding is discussed and the application of alternative primers suggested.
Highlights
Mitochondrial introns intermit coding regions of genes and feature characteristic secondary structures and splicing mechanisms
Mitochondrial intron diversity and characteristics in tetractinellid sponges The current study comprises the largest dataset of sponge mitochondrial introns to date (95 sequences of which 72 are new), encompassing 13 different sponge genera
This study provides novel insights into the taxonomic distribution, diversity and mobility of mitochondrial group I introns in sponges, and validates the subclass Spirophorina (Tetractinellida), as an intron hotspot in sponges, notably by increasing the number of Tetillidae introns known by a factor of 5
Summary
Mitochondrial introns intermit coding regions of genes and feature characteristic secondary structures and splicing mechanisms. Based on different insertion sites within the cox gene and secondary structures, four types of group I and two types of group II introns are known, which can harbor up to three encoding homing endonuclease genes (HEG) of the LAGLIDADG family (group I) and/or reverse transcriptase (group II). Group I and group II introns are distinguished based on their splicing mechanisms and secondary structures. II introns were observed within the core regions of their secondary structures. Group I and group II introns often contain open reading frames (ORFs) in their loop regions [70], which can encode for different site-specific homing endonuclease genes (HEGs). 12 out of 44 group I introns and only one out of six group II introns are located in the cytochrome c oxidase subunit 1 (cox1) gene [54], an acknowledged insertion hotspot for mt group I introns [23]
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