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

Abstract

Contrary to the early evidence, which indicated that the mitochondrial architecture in one of the two major annelida clades, Sedentaria, is relatively conserved, a handful of relatively recent studies found evidence that some species exhibit elevated rates of mitochondrial architecture evolution. We sequenced complete mitogenomes belonging to two congeneric shell-boring Spionidae species that cause considerable economic losses in the commercial marine mollusk aquaculture: Polydora brevipalpa and Polydora websteri. The two mitogenomes exhibited very similar architecture. In comparison to other sedentarians, they exhibited some standard features, including all genes encoded on the same strand, uncommon but not unique duplicated trnM gene, as well as a number of unique features. Their comparatively large size (17,673 bp) can be attributed to four non-coding regions larger than 500 bp. We identified an unusually large (putative) overlap of 14 bases between nad2 and cox1 genes in both species. Importantly, the two species exhibited completely rearranged gene orders in comparison to all other available mitogenomes. Along with Serpulidae and Sabellidae, Polydora is the third identified sedentarian lineage that exhibits disproportionally elevated rates of mitogenomic architecture rearrangements. Selection analyses indicate that these three lineages also exhibited relaxed purifying selection pressures.

ORFanes in mitochondrial genomes of marine polychaetePolydora

“…Isolation and sequencing of total genomic DNA from this specimen enabled assembly of the mitochondrial genome. In this genome, we found all standard metazoan protein-coding genes (PCGs), rRNAs, tRNAs, duplicated tRNAs, as well as four additional regions that were also previously found in P websteri, P brevipalpa , and P. hoplura species (Ye et al 2021;Lee& Lee 2022). Similar to other polychaetes, all genes were encoded on a single strand (Figure 1).…”

“…Recently, three complete mitogenomes of shell-boring Polydora species, P. websteri, P. brevipalpa , and P. hoplura , were sequenced (Ye et al 2021; Lee & Lee 2022). Analysis of two related species, P. websteri and P. brevipalpa , and comparisons to other sedentary animals showed that Polydora mitogenomes have some unusual features: the gene order has been changed, and there are four non-coding regions that are longer than 500 bp.…”

“…Analysis of four large NCRs in both genomes has shown that none of them exhibited sequence similarity to the nearby coding regions. At the same time, several open reading frames (ORFs) > 50 amino acid residues were detected in NCRs, but BLASTp analysis found no hits with known proteins for any of the putative protein products (Ye et al 2021). The mitogenome of P. hoplura has been shown to have similar architecture, including the presence of NCRs (Lee & Lee 2022).…”

The complete mitochondrial genome of Hemiclepsis yangtzenensis (Clitellata: Glossiphoniidae)

“…The nucleotide composition of the mitogenome was 37.66% T, 15.04% C, 35.21% A, and 12.09% G, with a strong A + T bias of 72.87%, which is similar to other annelids (Ye et al. 2021 ). The G + C content of protein-coding genes was 26.61% (length: 11,134 bp), tRNAs 26.79% (length: 1,407 bp), and rRNAs 53.54% (length: 1,903) ( Supplementary Data ).…”

ORFans in Mitochondrial Genomes of Marine Polychaete Polydora

“…The architecture of the annelid mitochondrial genome is generally well conserved ( Weigert et al 2016 ), with some notable exceptions, for example, Ramisyllis multicaudata from the family Syllide ( Aguado et al 2015 ). Moreover, recently three complete mitogenomes of shell-boring Polydora species (Spionidae family), Polydora websteri , Polydora brevipalpa , and Polydora hoplura , were sequenced ( Ye et al 2021 ; Lee and Lee 2022 ). Analysis of two related species, P. websteri and P. brevipalpa , and comparisons with other sedentary animals showed that Polydora mitogenomes have some unusual features: the gene order has been changed, and there are four NCRs that are longer than 500 base pairs (bp).…”