45 research outputs found

    Bacterial Endosymbiosis in a Chordate Host: Long-Term Co-Evolution and Conservation of Secondary Metabolism

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    <div><p>Intracellular symbiosis is known to be widespread in insects, but there are few described examples in other types of host. These symbionts carry out useful activities such as synthesizing nutrients and conferring resistance against adverse events such as parasitism. Such symbionts persist through host speciation events, being passed down through vertical transmission. Due to various evolutionary forces, symbionts go through a process of genome reduction, eventually resulting in tiny genomes where only those genes essential to immediate survival and those beneficial to the host remain. In the marine environment, invertebrates such as tunicates are known to harbor complex microbiomes implicated in the production of natural products that are toxic and probably serve a defensive function. Here, we show that the intracellular symbiont <i>Candidatus</i> Endolissoclinum faulkneri is a long-standing symbiont of the tunicate <i>Lissoclinum patella</i>, that has persisted through cryptic speciation of the host. In contrast to the known examples of insect symbionts, which tend to be either relatively recent or ancient relationships, the genome of <i>Ca.</i> E. faulkneri has a very low coding density but very few recognizable pseudogenes. The almost complete degradation of intergenic regions and stable gene inventory of extant strains of <i>Ca.</i> E. faulkneri show that further degradation and deletion is happening very slowly. This is a novel stage of genome reduction and provides insight into how tiny genomes are formed. The <i>ptz</i> pathway, which produces the defensive patellazoles, is shown to date to before the divergence of <i>Ca.</i> E. faulkneri strains, reinforcing its importance in this symbiotic relationship. Lastly, as in insects we show that stable symbionts can be lost, as we describe an <i>L. patella</i> animal where <i>Ca.</i> E. faulkneri is displaced by a likely intracellular pathogen. Our results suggest that intracellular symbionts may be an important source of ecologically significant natural products in animals.</p></div

    <i>Ca.</i> E. faulkneri genes that are more than 20% shorter than their homolog in BAL199 in at least one strain.

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    <p><i>Ca.</i> E. faulkneri genes that are more than 20% shorter than their homolog in BAL199 in at least one strain.</p

    Only one gene varies in length by more than 20% in <i>Ca.</i> E. faulkneri strains L2 and L5, and only a few are truncated by more than 20% versus their homologs in BAL199.

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    <p>Comparisons shown: (A) <i>Ca.</i> E. faulkneri L2 and L5, (B) <i>Ca.</i> E. faulkneri L2 and BAL199, and (C) <i>Ca.</i> E. faulkneri L5 and BAL199. Green lines denote a tolerance of ±20% of the <i>x</i>-axis variable. Note: the large PKS genes in the <i>ptz</i> pathway are omitted in order to avoid skewing the scale of axes in (A).</p

    Primers used in this study.

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    <p>Primers used in this study.</p

    The ten contigs assigned to the <i>Ca.</i> X. pacificiensis genome from the metagenomic assembly have similar nucleotide composition.

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    <p>Boxplots are shown comparing GC% (top left), GC2 (bottom left), GC4 (top right) and CAI (codon adaptation index <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080822#pone.0080822-Sharp1" target="_blank">[49]</a>, bottom right) in contigs assembled from metagenomic sequence obtained from <i>L. patella</i> animal L6 and assigned to <i>Ca.</i> X. pacificiensis. The sizes of the contigs are shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080822#pone-0080822-t006" target="_blank">Table 6</a>. Only Contig16 was found to have a statistically significant difference in nucleotide composition to any other contig (see Main Text, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0080822#pone.0080822.s002" target="_blank">Table S2</a>).</p

    <i>Ca.</i> X. pacificiensis possesses genes involved in various pathogenicity-related processes, while <i>Ca.</i> E. faulkneri lacks genes in these categories.

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    <p><i>Ca.</i> X. pacificiensis possesses genes involved in various pathogenicity-related processes, while <i>Ca.</i> E. faulkneri lacks genes in these categories.</p

    Pseudogenes in <i>Ca.</i> E. faulkneri L2 and L5.

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    <p>Pseudogenes in <i>Ca.</i> E. faulkneri L2 and L5.</p

    Orphan genesa in <i>Ca.</i> E. faulkneri strains L2 and L5.

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    <p>Orphan genesa in <i>Ca.</i> E. faulkneri strains L2 and L5.</p

    <i>Ca.</i> E. faulkneri strains have low coding density and possess the largest genomes lacking <i>ftsZ</i>, and <i>Ca.</i> E. faulkneri L2 has the largest genome also lacking <i>dnaA</i>.

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    <p>A set of symbionts and pathogens that live intracellularly and/or show signs of genome reduction are shown, in descending order of genome size. Shaded blue squares indicate the presence of <i>ftsZ</i> or <i>dnaA</i>. Note: All genomes included above are completed except for <i>Ca.</i> X. pacificiensis where the genome size plotted reflects the sum of contig sizes in the draft genome.</p

    Contig lengths in the assembly of <i>Ca.</i> X. pacificiensis.

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    <p>Contig lengths in the assembly of <i>Ca.</i> X. pacificiensis.</p