Dataset Information

Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae.

ABSTRACT: Chlamydiae are an example of obligate intracellular bacteria that possess highly reduced, compact genomes (1.0-3.5?Mbp), reflective of their abilities to sequester many essential nutrients from the host that they no longer need to synthesize themselves. The Chlamydiae is a phylum with a very wide host range spanning mammals, birds, fish, invertebrates, and unicellular protists. This ecological and phylogenetic diversity offers ongoing opportunities to study intracellular survival and metabolic pathways and adaptations. Of particular evolutionary significance are Chlamydiae from the recently proposed Ca. Parilichlamydiaceae, the earliest diverging clade in this phylum, species of which are found only in aquatic vertebrates. Gill extracts from three Chlamydiales-positive Australian aquaculture species (Yellowtail kingfish, Striped trumpeter, and Barramundi) were subject to DNA preparation to deplete host DNA and enrich microbial DNA, prior to metagenome sequencing. We assembled chlamydial genomes corresponding to three Ca. Parilichlamydiaceae species from gill metagenomes, and conducted functional genomics comparisons with diverse members of the phylum. This revealed highly reduced genomes more similar in size to the terrestrial Chlamydiaceae, standing in contrast to members of the Chlamydiae with a demonstrated cosmopolitan host range. We describe a reduction in genes encoding synthesis of nucleotides and amino acids, among other nutrients, and an enrichment of predicted transport proteins. Ca. Parilichlamydiaceae share 342 orthologs with other chlamydial families. We hypothesize that the genome reduction exhibited by Ca. Parilichlamydiaceae and Chlamydiaceae is an example of within-phylum convergent evolution. The factors driving these events remain to be elucidated.

SUBMITTER: Taylor-Brown A

PROVIDER: S-EPMC6171736 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae.

Taylor-Brown Alyce A Pillonel Trestan T Greub Gilbert G Vaughan Lloyd L Nowak Barbara B Polkinghorne Adam A

Genome biology and evolution 20181001 10

Chlamydiae are an example of obligate intracellular bacteria that possess highly reduced, compact genomes (1.0-3.5 Mbp), reflective of their abilities to sequester many essential nutrients from the host that they no longer need to synthesize themselves. The Chlamydiae is a phylum with a very wide host range spanning mammals, birds, fish, invertebrates, and unicellular protists. This ecological and phylogenetic diversity offers ongoing opportunities to study intracellular survival and metabolic p ...[more]

PMID: 30202970

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Project description:BackgroundFew, if any, protozoan parasites are reported to exhibit extreme organ tropism like the flagellate Tritrichomonas foetus. In cattle, T. foetus infects the reproductive system causing abortion, whereas the infection in cats results in chronic large bowel diarrhoea. In the absence of a T. foetus genome, we utilized a de novo approach to assemble the transcriptome of the bovine and feline genotype to identify host-specific adaptations and virulence factors specific to each genotype. Furthermore, a subset of orthologs was used to characterize putative druggable targets and expose complications of in silico drug target mining in species with indefinite host-ranges.ResultsIllumina RNA-seq reads were assembled into two representative bovine and feline transcriptomes containing 42,363 and 36,559 contigs, respectively. Coding and non-coding regions of the genome libraries revealed striking similarities, with 24,620 shared homolog pairs reduced down to 7,547 coding orthologs between the two genotypes. The transcriptomes were near identical in functional category distribution; with no indication of selective pressure acting on orthologs despite differences in parasite origins/host. Orthologs formed a large proportion of highly expressed transcripts in both genotypes (bovine genotype: 76%, feline genotype: 56%). Mining the libraries for protease virulence factors revealed the cysteine proteases (CP) to be the most common. In total, 483 and 445 bovine and feline T. foetus transcripts were identified as putative proteases based on MEROPS database, with 9 hits to putative protease inhibitors. In bovine T. foetus, CP8 is the preferentially transcribed CP while in the feline genotype, transcription of CP7 showed higher abundance. In silico druggability analysis of the two genotypes revealed that when host sequences are taken into account, drug targets are genotype-specific.ConclusionGene discovery analysis based on RNA-seq data analysis revealed prominent similarities between the bovine and feline T. foetus, suggesting recent adaptation to their respective host/niche. T. foetus represents a unique case of a mammalian protozoan expanding its parasitic grasp across distantly related host lineages. Consequences of the host-range for in silico drug targeting are exposed here, demonstrating that targets of the parasite in one host are not necessarily ideal for the same parasite in another host.

Dataset Information

Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae.

Publications

Metagenomic Analysis of Fish-Associated Ca. Parilichlamydiaceae Reveals Striking Metabolic Similarities to the Terrestrial Chlamydiaceae.

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