Putative cross-kingdom horizontal gene transfer in sponge (Porifera) mitochondria
© Rot et al; licensee BioMed Central Ltd. 2006
Received: 21 March 2006
Accepted: 14 September 2006
Published: 14 September 2006
The mitochondrial genome of Metazoa is usually a compact molecule without introns. Exceptions to this rule have been reported only in corals and sea anemones (Cnidaria), in which group I introns have been discovered in the cox1 and nad5 genes. Here we show several lines of evidence demonstrating that introns can also be found in the mitochondria of sponges (Porifera).
A 2,349 bp fragment of the mitochondrial cox1 gene was sequenced from the sponge Tetilla sp. (Spirophorida). This fragment suggests the presence of a 1143 bp intron. Similar to all the cnidarian mitochondrial introns, the putative intron has group I intron characteristics. The intron is present in the cox1 gene and encodes a putative homing endonuclease. In order to establish the distribution of this intron in sponges, the cox1 gene was sequenced from several representatives of the demosponge diversity. The intron was found only in the sponge order Spirophorida. A phylogenetic analysis of the COI protein sequence and of the intron open reading frame suggests that the intron may have been transmitted horizontally from a fungus donor.
Little is known about sponge-associated fungi, although in the last few years the latter have been frequently isolated from sponges. We suggest that the horizontal gene transfer of a mitochondrial intron was facilitated by a symbiotic relationship between fungus and sponge. Ecological relationships are known to have implications at the genomic level. Here, an ecological relationship between sponge and fungus is suggested based on the genomic analysis.
Sponges (Porifera) are the first diverging metazoans. They are thus a key phylum in the understanding of the genomic characteristics of the metazoan ancestor . For example, recent findings indicate that the sponge mitochondria possess ancestral characters that have been lost in other metazoans, such as additional genes, minimally modified genetic code, or bacteria-like rRNA structure [2, 3]. One intriguing finding is that most metazoan mitochondrial genomes lack introns. Mitochondrial introns may be present in large numbers and in many genes in the sister clades of Metazoa: Choanoflagellida , Ichthyosporea  and Fungi . For example, the mitochondrial genome of the fungi Podospora anserina (accession number: NC_001329) contains 33 introns located in nine different genes, including 15 introns in the cox1 gene, which encode the subunit 1 of cytochrome c oxidase (COI). However, none of these introns are obligatory and some fungi do not include introns in their mitochondrial genome (e.g., Schizophyllum commune, NC_003049; Harpochytrium sp. NC_004760 and NC_004623). In Metazoa, mitochondrial introns have only been described in Cnidaria of the subclass Zoantharia [6, 7]. In sea anemones (order Actinaria), two mitochondrial introns have been found, one in the cox1 gene and one in the NADH dehydrogenase subunit 5 gene (nd5). In stony corals (order Scleractinia), however, only the nd5 gene contains an intron. The relative position of this intron is conserved between sea anemone and stony corals. Other cnidarians (e.g., jellyfish, hydras) do not seem to possess mitochondrial introns [8, 9].
Mitochondrial introns are self-splicing ribozymes. Self-splicing introns are divided into either Group I or Group II depending on their secondary structure. While Group II introns are prevalent in plants, the mitochondrial introns of Cnidaria, Choanoflagellida and Ichtyosporea are all of group I. In the mitochondria of fungi both types of introns can be found, though group I is more prevalent . Self-splicing introns are mobile genetic elements [5, 10, 11]. They often encode homing endonucleases and/or maturases. Homing endonucleases cleave chromosomes and exploit the recombinational repair system of the cell for their multiplication. Maturases act as cofactors that bind the precursor RNA containing their intron to facilitate its folding and splicing . It should be noted that enzymes of the LAGLIDADG family (which are frequently encoded within group I introns) can function as endonuclease, as maturase, or perform both functions. However, not all introns encode homing endonuclease or maturase. For example, the peculiar intron located in the nd5 gene of cnidaria does not encode a homing endonuclease, although it encodes other mitochondrial genes [6, 7].
Although three mitochondrial genomes of sponges have been recently sequenced [2, 3], no intron was found in these genomes. We report here that a sponge mitochondrial gene contains a group I intron, which encodes a putative LAGLIDADG member. We also provide phylogenetic evidence suggesting that the sponge intron was acquired by horizontal gene transfer.
We amplified cox1 genes from nine demosponge species. All sponge species yielded similar cox1 PCR products (1206 bp) except Tetilla sp. (Spirophorida), whose product was much longer (2349 bp). Sequencing this gene revealed a putative intron of 1143 bp. This suggests that introns can also be found in the mitochondrial genome of sponges. Interestingly, the intron was located in the middle of the reverse primer used by Nichols et al.  to amplify cox1 gene of sponges. It is highly unlikely that the Tetilla cox1 sequence is a nuclear copy or a contamination, for three reasons: i. we extracted enriched mitochondrial DNA to avoid amplification of nuclear copies of mitochondrial sequences (Numts) ; ii. no frameshift mutations were noticeable in the cox1 sequence; and iii. an identical sequence was obtained from two individuals collected from separate locations.
Characteristics of the predicted Tetilla sp. intron
Mitochondrial introns often encode various proteins [7, 15]. Hence, the predicted Tetilla intron was translated in all six reading frames using the coelenterate/mold mitochondrial genetic code (i.e., the genetic code of sponge mitochondria). The translation revealed an open reading frame (ORF) of 1029 bp starting from the first nucleotide of the intron (the initiation codon is TTA). The main difference between the standard and the sponge mitochondrial genetic codes is that TGA codes for a stop codon in the standard genetic code while in the sponge mitochondria it codes for tryptophan. The intron ORF includes three TGA codons in positions 100, 169, and 631 of the intron sequence, indicating that the coding sequence of the intron is not of a nuclear origin.
The BLAST analysis of the ORF suggests that it encodes an enzyme from the LAGLIDADG endonuclease-maturase family. LAGLIDADG is the largest family of homing endonucleases, whose members are characterized by the presence of the conserved motif LAGLIDADG in one or two copies. Crystal structures of LAGLIDADG endonucleases-maturases have revealed that single-motif proteins function as homodimers while double-motif enzymes are monomers . Two LAGLIDADG motifs were identified in the Tetilla ORF (LAGLIEGDG and LAGFLDADG) located in positions 101–109 and 212–220 of the ORF protein sequence.
Phylogenetic tree of the COI protein sequence
Phylogenetic tree of the LAGLIDADG
Phylogenetic reconstructions indicate a complicated evolutionary history for these homing endonuclease sequences (Figure 5). Because the LAGLIDADG protein tree has little to do with the species tree it was impossible to define an outgroup. In the tree, the predicted Tetilla sequence is associated with the LAGLIDADG sequence located in the 4th cox1 intron of Smittium culisetae. However, these two sequences show only 57% of identity in the conserved part of the LAGLIDADG alignment and the support values are weak for this grouping (BP = 54 and PP = 0.94). Similarly, the LAGLIDADG sequence present in the sea anemone Metridium senile does not show any close relationship with any of the sequences present in the data bank. More generally, intron sequences present in the same gene or in closely-related organisms do not form monophyletic groups. For example, neither chloroplast sequences nor animal sequences clustered together. Only the plant sequences (BP = 100, PP = 1.0) and five nd5 sequences (BP = 97, PP = 1.0) form two coherent groups.
Insertion and deletion of mobile introns are common evolutionary events resulting in a sporadic distribution of these elements . Consequently, the presence of an intron in a lineage but not in its sister clades can always be explained by independent losses. However, three lines of evidence suggest that the predicted Tetilla sp. intron arose by horizontal gene transfer rather than by independent losses. First, parsimony analysis of intron presence and absence favors a scenario of a recent intron introduction in Spirophorida since all other ten sponges for which the cox1 gene was determined lack an intron (Figure 4). Second, the cnidarian intron is not located at the same position as the sponge intron, suggesting an independent evolutionary origin (Figure 1). Third, phylogenetic analyses clearly show that the intron-encoded LAGLIDADG sequence and the cox1 exonic sequence share different phylogenetic histories (Figures 4, 5). The Tetilla COI protein is of sponge origin and its phylogeny agrees with previous sponge molecular phylogeny [21, 25], while the LAGLIDADG-based phylogenetic tree indicates that the Tetilla intron ORF is closer to fungal than to cnidarian or choanoflagelate sequences (Figure 5). Thus, the intron might be of fungal origin.
It is unlikely that the intron was transferred from the nuclear genome. The ORF can be translated with the sponge/mold/cnidarian mitochondrial genetic code but not with the nuclear genetic code. The mitochondrial origin of this sequence is also supported by the fact that the ORF sequence is more similar to cox1 LAGLIDADG than to ribosomal LAGLIDADG (Figure 5).
We predicted the first sponge mitochondrial intron and our phylogenetic analyses indicate that it might have a fungal origin. A fungal origin implies that the sponge and the donor interacted in such a way as to allow the transfer of the intron. This suggests the existence of a symbiosis between Tetilla sp. and a fungus donor of the intron.
There is an increasing interest recently in marine fungi as a source of novel bioactive-compounds . More than 500 species of marine fungi, mainly Ascomycota, have been described [27, 28] and the number is constantly rising [29–31]. Unfortunately, no cox1 gene has yet been sequenced from marine derived fungi. In the marine environment, fungi have been isolated from sediments, algae, plants, fish, crabs, tunicates, corals, and sponges [26, 32]. In spite of the fact that many fungi had been isolated from sponges [32–35], the existence of a sponge-fungus symbiosis is under debate. No fungi had been observed within a sponge and it was therefore supposed that only dormant fungi propagules are present within sponges. The first clear case of an endosymbiotic yeast was recently discovered in sponges of the genus Chondrilla . Additionally, another recent molecular study gave the first proof that sponges have the ability to recognize fungi in their surrounding environment . Our results thus introduce additional evidence in favor of a sponge-fungus symbiosis.
Because horizontal gene transfers of group I introns encoding LAGLIDADG are frequent among fungi, we could not determine which lineage of fungi was at the origin of the sponge intron. The sponge LAGLIDADG sequence clusters with the LAGLIDADG present in the fourth cox1 intron of Smittium culisetae. However, the location of the LAGLIDADG ORF is different in these two introns (Figure 3). Most of the ORF is located in the paired region P8 in Tetilla while in Smittium it is located before the paired region P3. This suggests that the ORF and the rest of the intron (i.e., the ribozyme component) have independent origins, thus complicating our understanding of the sponge intron origin. Because the diversity of marine organisms is still poorly known and because sponges are remarkable for their widespread symbiosis with various organisms [38, 39], we cannot exclude the hypothesis that an unknown unicellular eukaryote was the donor of the intron. The accumulation of new data on marine fungi mitochondrial genomes is likely to shed additional light on the sponge intron origin and perhaps also on the origin of the LAGLIDADG sequence in Cnidaria.
Our analysis suggests that a cross-kingdom horizontal gene transfer event occurred in the sponge mitochondrial genome. Such events are remarkable from the evolutionary point of view, because they demonstrate an unexpected plasticity of the mitochondrial genomes of basal Metazoa compared to the more conserved genomes of Bilateria. Porifera and Cnidaria mtDNAs have been characterized by the presence of additional horizontally-transferred genes [6, 40], introns [6, 7], tRNA duplications , and tRNA losses [7, 41]. Our results suggest that a better sampling of these animals might improve our understanding of the evolution of this genome.
There are many exciting evolutionary events in marine organisms that are only now starting to be discovered, and these events will provide new insights concerning the evolution of the animal kingdom. Ecological relationships are known to have implications at the genomic level. Here, an ecological relationship between a sponge and a fungus (or an unknown eukaryote) is suggested, based on the genomic analysis.
DNA extraction and amplification
Eight sponge species were collected and identified by traditional morphological taxonomy based on their general morphology and skeletal organization. Total DNA extractions from the sponge species Xestospongia proxima, Biemna fistulosa, Cliona sp., Verongula giganthea, and Aplysina lacunosa were performed following Steindler et al. . For Tetilla sp., Negombata magnifica, and Chondrosia reniformis, an enriched fraction of mitochondrial genomes was extracted following Arnason et al. . This protocol reduces the chance of Numt contamination.
The primers LCO1490  and COX1-R1 (5'-TGTTGRGGGAAAAARGTTAAATT-3') were used to amplify the cox1 gene. The conditions of PCR amplifications were: 1 cycle at 94°C for 2 min, 50°C for 1 min, 72°C for 2 min; 30 cycles at 94°C for 50 sec, 50°C for 50 sec, 72°C for 2 min; and a final elongation at 72°C for 10 min. Amplified fragments were directly sequenced on an ABI PRISM 3100 (Applied Biosystems). Internal primers are provided in Additional file 2.
Intron location and structure were inferred in silico. The core structure of the intron was inferred with the program CITRON  and manually aligned with fungal and metazoan introns on the basis of secondary structure prediction. The fungal species chosen were the closest based on the phylogenetic analyses of LAGLIDADG sequences. The structure of other regions (i.e., P1, P5, P6, P9) was predicted using the program Mfold .
COI taxa sampling
Sequences were aligned using ProbCons  with three consistency steps and 500 iterative refinement repetitions. The alignments were then corrected by hand and gaps present in more than 25% of the taxa were removed from the analyses. The COI corrected alignment comprised 24 species and 400 characters while the LAGLIDADG data set comprised 89 sequences and 263 characters. Both alignments are provided as Additional files 3 and 4. For each data set two analyses were conducted: a maximum likelihood analysis with the program PHYML v2.4.4  and a Bayesian analysis with the program MrBayes3.1 . Both analyses were done using the mtREV amino-acid replacement model . Among-site rate variation was represented by a gamma distribution  with eight categories and a proportion of invariant sites for the COI data set. The proportion of invariant sites was set to zero for the LAGLIDADG analysis because preliminary analysis with PHYML had estimated the proportion of invariant sites to be very small. For maximum likelihood analyses, bootstrap percentages were computed using 1000 replicates for the COI data set and 500 replicates for the LAGLIDADG data set. The Bayesian analyses were performed with two independent runs. For each run, four chains were sampled every 100 generations. Each chain was run for 5,000,000 or 6,000,000 generations for the COI and the LAGLIDADG data set respectively. Clade posterior probabilities (PP) were calculated after removal of the first 12,500 trees for the COI analysis (burnin). In this case, the average standard deviation of split frequencies was below 0.01 before the burnin threshold, and the potential scale reduction factors of the parameters were equal to 1. This indicates that the run had probably converged. For the LAGLIDADG analysis, the average standard deviation of split frequencies was below 0.01 after 5,100,000 generations. Consequently, the first 51,000 trees were removed before computation of the clade posterior probabilities.
We would like to thank Laura Steindler for her help with sponge DNA extraction, and Sara Kinamon for her help in the laboratory. Three anonymous reviewers provided valuable comments. Sponge tissue samples are part of the museum collections of Tel-Aviv University.
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