Multiple introns in a deep-sea Annelid (Decemunciger: Ampharetidae) mitochondrial genome

Abstract

Wood falls provide episodic fluxes of energy to the sea floor that are degraded by a species-rich benthic fauna. Part of this rich diversity includes annelid polychaetes but unfortunately, our understanding of such fauna is limited and their genetic variability and evolutionary origins remain poorly known. In this study, we sequenced complete mitochondrial genomes from three congeneric Decemunciger (Ampharetidae) individuals that had colonized multiple wood falls in the deep (~1600 m) NE Pacific Ocean. Mitochondrial gene order within Decemunciger was similar to the three other available Terebellomorpha genomes, consistent with the relatively conserved nature of mitochondrial genomes within annelids. Unexpectedly, we found introns within the cox1, nad1 and nad4 genes of all three genomes assembled. This is the greatest number of introns observed in annelid mtDNA genomes, and possibly in bilaterians. Interestingly, the introns were of variable sizes suggesting possible evolutionary differences in the age and origins of introns. The sequence of the introns within cox1 is similar to Group II introns previously identified, suggesting that introns in the mitochondrial genome of annelids may be more widespread then realized. Phylogenetically, Decemunciger appears to be a sister clade among current vent and seep deep-sea Ampharetinae.

Mitochondrial genomes of two Polydora (Spionidae) species provide further evidence that mitochondrial architecture in the Sedentaria (Annelida) is not conserved

“…Only 5 sedentarian mitogenomes were larger: Spirobranchus giganteus 16 , Siboglinium fiordicum 29 and three Decemunciger sp. mitogenomes 30 . Both Polydora species possess the standard set of 37 genes, plus a duplicated trnM gene copy between trnL1 and nad1 (Fig.…”

“…The previous observation that S. spallanzanii has genes encoded on both mitochondrial strands raises intriguing questions about the evolution of mitochondrial transcription mechanism in Annelida 11 , as Boore proposed a ‘ratchet’ effect that would constitute a barrier to further strand switches once the replication mechanism has been lost on one strand 40 . As introns were described in mitochondrial genes of three separate annelid lineages so far 30 , 44 , 45 , this implies that mitochondrial evolution in Sedentaria deserves more scientific attention than it is currently receiving and that further annelid mitogenomes should be sequenced in order to further elucidate the intriguing patterns of mitogenomic evolution in this class.…”

Two new deep-water species of Ampharetidae (Annelida: Polychaeta) from the eastern Australian continental margin

“…Our results contradict Kongsgrud et al (2017) which recovered Ampharetidae as monophyletic with Samythella neglecta nested within Ampharetinae (posterior probability 0.78 for the Ampharetinae clade from combined COI, 16S and 18S tree). Ampharetinae was also recovered as monophyletic with high support, in Bernardino et al (2017) using protein-coding and mitochondrial genes and in Stiller et al (2013) using the COI, 16S, 18S gene fragments, however, both studies did not include Samythella sequences in their datasets. In Eilertsen et al (2017), the position of Samythella neglecta varied between gene trees: in the concatenated gene tree (COI, 16S, 18S, 28S) Samythella was recovered as the sister group to the rest of Ampharetidae and Avinellidae with high support (posterior probabilities (PP) = 1, bootstrap values (BS) = 83) also in the COI and 18S gene trees Samythella was recovered outside Ampharetinae and sister to Melinninae (COI: PP < 0.75/ BS < 50, 18S: PP 0.98/ BS 53), whilst in the 16S and 28S gene trees it was recovered within Amphretinae (16S: PP 0.94/ BS 48, 28S: 0.57/ BS 76).…”

“…The molecular phylogenetic studies on the family Ampharetidae (Bernardino et al, 2017;Eilertsen et al, 2017;Kongsrud et al, 2017;Parapar et al, 2018;Stiller et al, 2013;Zhong et al, 2011;Zhou et al, 2019) have focused on species within Ampharetinae, only one (Bernardino et al, 2017;Stiller et al, 2017) or two species (Eilertsen et al, 2017) of Melinninae were included in each dataset. Recently, Stiller et al (2020) included six species of Melinninae in their phylogeny of all Terebelliformia.…”

Organellar Introns in Fungi, Algae, and Plants

“…Group I introns are widespread and have been reported from nuclear rDNA (18S and 26S RNA genes) in fungi, protozoans, metazoans [36][37][38][39][40][49][50][51][52][53][54][55][56][57][58], bacterial genomes, phages and viruses, archaeal genomes, and they are encountered frequently in mitochondrial and plastid genomes (reviewed in [59]). With regard to metazoans, Group I introns have been noted in the mitochondrial genomes in members of Placozoa, Anthozoa, and Porifera [54,56,57].…”