Evolution of group I introns in Porifera: new evidence for intron mobility and implications for DNA barcoding.
Mitochondrial 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.



For 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.



This 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.
Department of Earth- & Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333, Munich, Germany.
Astrid
A
Schuster
Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, Dania Beach, FL, 33004, USA.
Jose V
JV
Lopez
Marine Animal Ecology, Wageningen University & Research Centre, P.O. Box 3700, AH, Wageningen, The Netherlands.|Naturalis Biodiversity Center, Marine Zoology Department, PO Box 9517, 2300, RA, Leiden, The Netherlands.
Leontine E
LE
Becking
National Centre for Aquatic Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research, P.O. Box 109-695, Newmarket, Auckland, New Zealand.
Michelle
M
Kelly
Harbor Branch Oceanographic Institute-Florida Atlantic University, 5600 U.S. 1 North, Ft Pierce, FL, 34946, USA.
Shirley A
SA
Pomponi
Department of Earth- & Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333, Munich, Germany.|SNSB - Bavarian State Collections of Palaeontology and Geology, Richard-Wagner Str. 10, 80333, Munich, Germany.|GeoBio-CenterLMU, Ludwig-Maximilians-Universität München, Richard-Wagner Str. 10, 80333, Munich, Germany.
Gert
G
Wörheide
Department of Earth- & Environmental Sciences, Palaeontology and Geobiology, Ludwig-Maximilians-Universität München, Richard-Wagner-Str. 10, 80333, Munich, Germany. erpenbeck@lmu.de.|GeoBio-CenterLMU, Ludwig-Maximilians-Universität München, Richard-Wagner Str. 10, 80333, Munich, Germany. erpenbeck@lmu.de.
Dirk
0000-0003-2716-1085
D
Erpenbeck
Department of Medicinal Chemistry, Division of Pharmacognosy, BioMedical Center, Uppsala University, Husargatan 3, 75123, Uppsala, Sweden. paco.cardenas@fkog.uu.se.
Paco
P
Cárdenas
D000818:Animals; D001483:Base Sequence; D005075:Biological Evolution; D058893:DNA Barcoding, Taxonomic; D004720:Endonucleases / Q000235:genetics; D007438:Introns; D008928:Mitochondria / Q000235:genetics; D016366:Open Reading Frames; D010802:Phylogeny; D011161:Porifera / Q000145:classification / Q000235:genetics*; D012326:RNA Splicing
D004720:Endonucleases
DNA barcoding; HGT; LAGLIDADG; Porifera; Tetractinellida; VGT; cox1; group I intron; homing endonuclease gene (HEG)