Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha

- Extensive gene rearrangements in the mitogenomes of congeneric annelid.
- species and insights on the evolutionary history of the genus Ophryotrocha.
- In addition, we investigated the evolution of the reproductive mode in the Ophryotrocha genus using a phylogeny based on two mitochondrial markers (COXI and 16S rDNA) and one nuclear fragment (Histone H3)..
- However, this separation was not observed in the phylogeny based on the COX1, 16S rDNA, and H3 genes.
- The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material.
- For similar reasons, the interstitial worms in the genus Ophryotrocha Claparède &.
- As new areas in the sea are explored, new Ophryotrocha species are regularly discovered and described [39–46], and with them the need to clarify the phylogenetic relationships within this genus.
- In order to improve our knowledge on the evolutionary history of the genus Ophryotrocha, we: (i) characterised for the first time the complete mitochondrial genomes of six Ophryotrocha species (Ophryotrocha adherens Paavo, Bailey-Brock &.
- Åkesson, 2010), (ii) compared the gene orders of the six species with those de- scribed for the main annelids’ taxonomic groups, (iii) used these novel mitogenomes to investigate the phylogenetic relationships among the six corresponding Ophryotrocha species and, finally, (iv) updating the Ophyrotrocha phyl- ogeny to portray how reproductive mode may be linked to evolutionary history in this genus..
- We succeeded Table 1 Sequencing characteristics of the six Ophryotrocha species investigated.
- Most of the genes started with the ATG codon and finished with the TAA stop codon (Table 2).
- Most of the PCG in each Ophryotrocha species harboured negative AT-skew (Table 3), suggesting a bias in T, with the exception of seven PCG in O.
- Positive values of AT-skew were observed in the ribosomal genes of five Ophryotrocha species, indi- cating a bias in A.
- The length of the small ribosomal unit varied between 736 bp (O.
- adherens), while that of the large ribosomal subunit ranged between 1064 bp (O.
- 1 Mitochondrial genome of the six Ophryotrocha species.
- The orientation of the arrows represents the orientation of the gene.
- Table 2 Codon usage in the 13 PCG for each of the six Ophryotrocha species investigated RSCU.
- In the remaining Ophryotrocha species, Valine and Glu- tamate were not found, while Aspartate was missing only in O.
- NAD1, NAD2, NAD3 and a reversion of the two riboso- mal genes.
- diadema differed by three transpositions of NAD5, ATP8 and the block of NAD1, NAD2 and NAD3 genes, and a reversion of the ribosomal genes.
- japonica differed by a tandem duplication random loss of ATP8 and a transposition of the 16S, NAD1, NAD3.
- Ophryotrocha diadema and the Ampharetidae gene order were similar and differed by the position of NAD1, NAD2, NAD3 and the reversal of the two ribosomal genes.
- labronica gene order differed by the transposition of the COX2, ATP8, COX3, NAD6, CYTB, ATP6 and NAD5 regions.
- Table 2 Codon usage in the 13 PCG for each of the six Ophryotrocha species investigated (Continued) RSCU.
- Mitochondrial phylogeny of the six studied Ophryotrocha species.
- The concatenation of the amino-acid sequences resulted in a fragment of 4098 residues.
- The concatenation of the nucleo- tide sequences resulted in a fragment of 12,297 bp.
- 2 PCG gene order and ribosomal RNAs of the Ophryotrocha species studied and other annelids.
- japonica, only the gene order of the latter was displayed.
- The up and down blocks represent the position on the plus or the minus strand of the gene.
- Ophryotrocha genus phylogeny and ancestral state reconstruction of the reproductive mode.
- adherens and species of the O.
- In the BI phylogeny, the species O.
- in a specific clade as observed in the ML phylogeny (aLTR = 83)..
- In the phylogeny of the Ophryotrocha genus, we iden- tified 25 gonochoric species, seven protandrous herm- aphrodite species and 11 simultaneous hermaphrodite species.
- However, for the protandrous group containing all the Ophryotrocha puerilis species and the gonochoric species Ophryotrocha eutrophila, the support of the ancestral state was low (pp <.
- 4 Maximum likelihood phylogeny of the genus Ophryotrocha based on the fragment of COXI, 16S and H3 under the GTR model with invariant gamma sites and ancestral state reconstruction.
- 5 Bayesian phylogeny of the genus Ophryotrocha based on the fragments of COXI, 16S and H3 under the GTR model with invariant gamma sites and ancestral state reconstruction.
- Colors of the branch represent the reproductive mode for all the species and their common ancestors: light blue (protandrous hermaphrodite), dark blue (simultaneous hermaphrodite), pink (gonochoric) and grey for unknown mode.
- ancestral state reconstruction of the reproductive mode shows that gonochorism is the plesiomorphic condition in the Ophryotrocha genus, not hermaphroditism as pre- viously hypothesized.
- Below we discuss in detail these major findings, and their implications for understanding the molecular evolution of the mitochondrial genome within the genus Ophryotrocha..
- Genome organisation and features of the six Ophryotrocha species.
- Their AT-content, AT and GC-skew, the length of the ribosomal genes and the ini- tiative codons of the PCG are congruent with those re- ported for other annelids and metazoans [55].
- Surprisingly, the gene order of the mitochondrial gen- ome was not conserved as the positions of PCG and tRNA differed among the six Ophryotrocha species..
- Usually, all annelid mitochondrial genes are encoded on the same strand except in the tubeworm Owenia fusiformis, the magelonid Magelona mirabilis (Johnston, 1865), and the ragworm Laeonereis culveri (Webster, 1879), which have one or two tRNA located on the minus strand [12, 67].
- To explain this, it was hypothesised that, in the last common ancestor of annelids, all the genes were encoded on the same strand by chance wherein a ratchet effect took place, eliminat- ing all the transcriptional elements and preventing the translocation of genes to the other strand [1, 68].
- The first hypothesis implies that in the last common ancestor of annelids, a single strand first encoded all genes and then underwent an inversion-transposition of the tRNAs and their transcriptional elements.
- Indeed, sequencing strategies and/or annotation meth- odologies can influence the results in terms of length of the mitogenome sequence recovered or in the gene length [69].
- Some studies have documented the presence of dissimilarities in the assembly and annotation of mito- chondrial genomes that are not always associated with low coverage [69, 70].
- Based on our first mitogenome phylogeny of the genus Ophryotrocha, the two main clusters differed in their sexual strategies: one group including only gonochoric species (O.
- values in most of the PCG and ribosomal genes, as re- ported for other mitogenomes of annelids [50]..
- Based on the phylogeny of the Ophryotrocha genus we obtained, two main clades were identified: clade 1 that contains most of gonochoric species and clade 2 mostly composed of hermaphrodite species, but also including species with gonochoric strategies.
- The separation of this clade was not linked to the reproductive mode of the species, although most of them are lacking information on their reproductive mode.
- In certain cases, the wrong taxonomic identification of the species may have occurred, prompting the incorrect as- sociation to a given reproductive mode, such as for se- quences labeled as O.
- Finally, we confirmed that Iphitime species do cluster in the Ophryotrocha genus .
- socialis, whereas in the phylogeny from Heggoy et al.
- As reported in previous studies, three different repro- ductive modes are present in the Ophryotrocha genus, i.e.
- Indeed, both gonochoric and hermaphroditic spe- cies of the Ophryotrocha genus show some degree of sexual lability in the population that can potentially favour the expression of alternative reproductive strat- egies [76].
- In particular, the presence of sexual pheno- types in the gonochoric species (i.e.
- In the Medi- terranean Sea, the gonochoristic species O.
- However, the lack of information on environmental population densities and on life history for the majority of the Ophryotrocha species comprising our phylogeny prevents this hypothesis from being formally tested..
- Finally, developing an in-depth genomic understanding of the Ophryotrocha genus will help further the investigation of both evolution of life-history traits and the emerging field of evolution- ary global change biology .
- Specimen collection, genomic extractions and sequencing Specimens of the six Ophryotrocha species originated from individuals collected in 2008 (O.
- adherens) in the harbour of Porto Empedocle (Italy.
- puerilis) in the harbour of La Spezia (Italy N E).
- The libraries were quantified and pooled using an equimolar ratio and se- quenced on an Illumina MiSeq 300 base-pair (bp) paired- end run (600 cycle, v3 kit) at the Plateforme d’Analyses Génomiques of the Institut de Biologie Intégrative et des Systèmes (Laval University, Quebec, Canada)..
- The quality of the sequencing was assessed with Fastqc [83], and adapters were removed with Trimmomatic [84] available in usegalaxy.org [85].
- Deter- mination of the A + T content of protein-coding genes, tRNA genes, rRNA genes and the RSCU was performed with DAMBE 6 [91].
- Two species were used as outgroup in the phylogenies: Marphysa sanguinea (NC_023124.1) and O.
- The significance of the test was performed with a 1000 permutations.
- In addition to the maximum parsimony reconstruc- tion, we also used a method based on Bayesian MCMC sampling methods to reconstruct the ancestral repro- ductive mode of the genus Ophryotrocha as imple- mented in BEAST2 [108].
- In particular, we used the Bayesian phylogeny previously obtained and estimate the posterior probability of the state for each ancestor for each node of the tree.
- Matrix of the comparison between gene order of the six Ophryotrocha species investigated..
- Matrix of the comparison between gene order of Ophryotrocha and other annelids..
- We would like to thank Marie-Hélène Carignan for her help in the laboratory and Dr.
- This work was realized with the financial support of (i) a UQAR BORÉAS collaborative research program and a QCBS Seed Grant (#56 entitled « Mitogenomics of polychaete worms of the Ophryotrocha genus: an emerging model for multigenerational experiments in marine invertebrates.
- (iii) a Natural Sciences and Engineering Research Council of Canada Discovery Program grant (RGPIN the Programme Établissement de Nouveaux Chercheurs Universitaires of the Fonds de Recherche du Québec — Nature et Technologies (No.199173), and the Fonds de recherche de l ’ Université du Québec à Rimouski, all awarded to PC.
- All mitochondrial sequences and the Histone 3 fragment were deposited under the accession number MT737360-MT737365 and MT733538-MT733543 in the Genbank database.
- The accession number of all sequences of COI, 16S and H3 used in this study are listed in the additional file 16 of the Supplementary Material and are available in Genbank database.
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