The mitochondrial genomes of sponges provide evidence for multiple invasions by Repetitive Hairpin-forming Elements (RHE)

Abstract

Background: The mitochondrial (mt) genomes of sponges possess a variety of features, which appear to be intermediate between those of Eumetazoa and non-metazoan opisthokonts. Among these features is the presence of long intergenic regions, which are common in other eukaryotes, but generally absent in Eumetazoa. Here we analyse poriferan mitochondrial intergenic regions, paying particular attention to repetitive sequences within them. In this context we introduce the mitochondrial genome of Ircinia strobilina (Lamarck, 1816; Demospongiae: Dictyoceratida) and compare it with mtDNA of other sponges.

Results: Mt genomes of dictyoceratid sponges are identical in gene order and content but display major differences in size and organization of intergenic regions. An even higher degree of diversity in the structure of intergenic regions was found among different orders of demosponges. One interesting observation made from such comparisons was of what appears to be recurrent invasions of sponge mitochondrial genomes by repetitive hairpin-forming elements, which cause large genome size differences even among closely related taxa. These repetitive hairpin-forming elements are structurally and compositionally divergent and display a scattered distribution throughout various groups of demosponges.

Conclusion: Large intergenic regions of poriferan mt genomes are targets for insertions of repetitive hairpin- forming elements, similar to the ones found in non-metazoan opisthokonts. Such elements were likely present in some lineages early in animal mitochondrial genome evolution but were subsequently lost during the reduction of intergenic regions, which occurred in the Eumetazoa lineage after the split of Porifera. Porifera acquired their elements in several independent events. Patterns of their intra-genomic dispersal can be seen in the mt genome of Vaceletia sp.

Figure 1

Dictyoceratida mtDNA. Schematic and linearized view of the three dictyoceratid mt genomes. The grey vertical bars indicate IGRs of high similarity between the taxa as connected by grey lines. Coloured horizontal bars (also highlighted with triangles and motif names) indicate repetitive regions inside the genomes. Coloured vertical bars (also highlighted with triangles and motif names) inside the genomes display putative RHEs. Their corresponding secondary structure and alignment is provided inside the boxes of the same colour. The GC-content of the Vaceletia mt genome is indicated by the black field below the structure. The numbers in the sequence names refer to their position in the mt genome. The numbers at the structures refer to their position in the alignments.

Figure 2

RHEs in miscellaneous demosponges. Secondary structures and their corresponding alignments of RHEs in A) Igernella notabilis (Dendroceratida), B) Halisarca dujardini (Halisarcida), C) Aplysina fulva (Verongida) and D) Ephydatia muelleri (Spongillina). The numbers in the sequence names refer to their position in the mt genome. The numbers at the structures refer to their position in the alignments. The black box indicates the particular fragment region for which the secondary structure is given. Alignable flanking regions are displayed.

Figure 3

RHEs in the demosponge Axinella corrugata. Secondary structures and their corresponding alignments of RHEs in Axinella corrugata (Halichondrida). The numbers in the sequence names refer to their position in the mt genome. The numbers at the structures refer to their position in the alignments. The black box indicates the particular fragment region for which the secondary structure is given. Alignable flanking regions are displayed.

Figure 4

RHEs in the demosponge Suberites domuncula. Secondary structures and their corresponding alignments of RHEs in Suberites domuncula (Hadromerida). The numbers in the sequence names refer to their position in the mt genome. The numbers at the structures refer to their position in the alignments. The black box indicates the particular fragment region for which the secondary structure is given. Alignable flanking regions are displayed.

Figure 5

Phylogenetic tree reconstructed from the protein coding genes of the mt genomes analysed. Phylogenetic tree reconstructed from the protein coding genes. The coloured boxes following the taxon names comprise the numbers and ratios of nucleotides in the IGRs. Green boxes: presence of significant RHEs; orange boxes; presence of repetitive elements in very low copy numbers; red boxes: no RHEs; uncoloured boxes: undecided due to incomplete sequences. The numbers following the taxon names indicate the GenBank accession numbers. Numbers on the branches are Bayesian posterior probabilities. The asterisks at hexactinellid taxa denote incompletely sequenced genomes. Please note that the long branch of Hexactinellida might influence branching pattern and higher support values (refer to [5,29,30]).