Distinctive Expansion of Potential Virulence Genes in the Genome of the Oomycete Fish Pathogen Saprolegnia parasitica

Broad Institute of MIT and Harvard, Cambridge, Massachusetts, United States of America.
PLoS Genetics (Impact Factor: 7.53). 06/2013; 9(6):e1003272. DOI: 10.1371/journal.pgen.1003272
Source: PubMed


Oomycetes in the class Saprolegniomycetidae of the Eukaryotic kingdom Stramenopila have evolved as severe pathogens of amphibians, crustaceans, fish and insects, resulting in major losses in aquaculture and damage to aquatic ecosystems. We have sequenced the 63 Mb genome of the fresh water fish pathogen, Saprolegnia parasitica. Approximately 1/3 of the assembled genome exhibits loss of heterozygosity, indicating an efficient mechanism for revealing new variation. Comparison of S. parasitica with plant pathogenic oomycetes suggests that during evolution the host cellular environment has driven distinct patterns of gene expansion and loss in the genomes of plant and animal pathogens. S. parasitica possesses one of the largest repertoires of proteases (270) among eukaryotes that are deployed in waves at different points during infection as determined from RNA-Seq data. In contrast, despite being capable of living saprotrophically, parasitism has led to loss of inorganic nitrogen and sulfur assimilation pathways, strikingly similar to losses in obligate plant pathogenic oomycetes and fungi. The large gene families that are hallmarks of plant pathogenic oomycetes such as Phytophthora appear to be lacking in S. parasitica, including those encoding RXLR effectors, Crinkler's, and Necrosis Inducing-Like Proteins (NLP). S. parasitica also has a very large kinome of 543 kinases, 10% of which is induced upon infection. Moreover, S. parasitica encodes several genes typical of animals or animal-pathogens and lacking from other oomycetes, including disintegrins and galactose-binding lectins, whose expression and evolutionary origins implicate horizontal gene transfer in the evolution of animal pathogenesis in S. parasitica.

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Available from: Berend Snel
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    • "To identify the ancestral oomycete secretome (AOS) we analyzed the three saprolegnian taxa in comparison with seven sequenced members of the Peronosporaleans. Collectively, these species represent a wide range of oomycete lifestyles, from free-living saprobes to obligate parasites of plants (table 2; Haas et al. 2009; Levesque et al. 2010; Raffaele et al. 2010; Links et al. 2011; Jiang et al. 2013). Using the secretome of the putative sister group of the oomycetes, Hyphochytridiomycete, Hyp. "
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    ABSTRACT: Saprotrophic and parasitic microorganisms secrete proteins into the environment to breakdown macromolecules and obtain nutrients. The molecules secreted are collectively termed the 'secretome' and the composition and function of this set of proteins varies depending on the ecology, life cycle, and environment of an organism. Beyond the function of nutrient acquisition, parasitic lineages must also secrete molecules to counteract host defenses. Here we use a combination of de-novo genome and transcriptome sequencing and bioinformatic identification of signal peptides to identify the putative secreted proteome of two oomycetes, the facultative parasite Achlya hypogyna and free-living Thraustotheca clavata. By comparing the secretomes of these saprolegnialean oomycetes with that of 8 other oomycetes, we were able to characterize the evolution of this protein set across the oomycete clade. These species span the last common ancestor of the two major oomycete families allowing us to identify the ancestral secretome. This ancestral secretome consists of at least 84 gene families that encode putatively secreted proteins. Only 11 of these gene families are conserved across all 10 secretomes analysed and the two major branches in the oomycete radiation. Notably, we have identified expressed elicitin-like effector genes in the saprotrophic decomposer, T. clavata. Phylogenetic analyses show six novel HGTs to the oomycete secretome from bacterial and fungal donor lineages, four of which are specific to the Saprolegnialeans. Comparisons between free-living and pathogenic taxa highlight the functional changes of oomycete secretomes associated with shifts in lifestyle. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Full-text · Article · Dec 2014 · Genome Biology and Evolution
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    • "Particularly for the modern plant pathogenic oomycetes, both fossil and molecular clock evidence suggests that the major lineages of angiosperms had diversified by the mid-Cretaceous [52], prior to our estimates for divergences among the peronosporaleans. The evolution of pathogenic lifestyles, therefore, may have been in response to certain environmental changes, or may have been facilitated by the horizontal transfer of pathogenicity-related genes from true Fungi [53-55] or from bacteria [45,56], as has been suggested previously. "
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    ABSTRACT: Background Molecular clock methodologies allow for the estimation of divergence times across a variety of organisms; this can be particularly useful for groups lacking robust fossil histories, such as microbial eukaryotes with few distinguishing morphological traits. Here we have used a Bayesian molecular clock method under three distinct clock models to estimate divergence times within oomycetes, a group of fungal-like eukaryotes that are ubiquitous in the environment and include a number of devastating pathogenic species. The earliest fossil evidence for oomycetes comes from the Lower Devonian (~400 Ma), however the taxonomic affinities of these fossils are unclear. Results Complete genome sequences were used to identify orthologous proteins among oomycetes, diatoms, and a brown alga, with a focus on conserved regulators of gene expression such as DNA and histone modifiers and transcription factors. Our molecular clock estimates place the origin of oomycetes by at least the mid-Paleozoic (~430-400 Ma), with the divergence between two major lineages, the peronosporaleans and saprolegnialeans, in the early Mesozoic (~225-190 Ma). Divergence times estimated under the three clock models were similar, although only the strict and random local clock models produced reliable estimates for most parameters. Conclusions Our molecular timescale suggests that modern pathogenic oomycetes diverged well after the origin of their respective hosts, indicating that environmental conditions or perhaps horizontal gene transfer events, rather than host availability, may have driven lineage diversification. Our findings also suggest that the last common ancestor of oomycetes possessed a full complement of eukaryotic regulatory proteins, including those involved in histone modification, RNA interference, and tRNA and rRNA methylation; interestingly no match to canonical DNA methyltransferases could be identified in the oomycete genomes studied here.
    Full-text · Article · May 2014 · BMC Evolutionary Biology
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    • "To infer homology within and across genomes of six divergent Phytophthora lineages and distantly related oomycetes (fig. 1) (Tyler et al. 2006; Haas et al. 2009; Baxter et al. 2010; Lévesque et al. 2010; Lamour et al. 2012; Jiang et al. 2013), we clustered all predicted proteins based on sequence similarity (see supplementary materials and methods, Supplementary Material online). Using the resulting gene families, we identified 2HOM blocks in the Phytophthora species and subsequently screened the other oomycetes for copies of these 2HOM blocks. "
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    ABSTRACT: Genomes of the plant-pathogenic genus Phytophthora are characterized by small duplicated blocks consisting of two consecutive genes (2HOM blocks) and by an elevated abundance of similarly aged gene duplicates. Both properties, in particular the presence of 2HOM blocks, have been attributed to a whole-genome duplication (WGD) at the last common ancestor of Phytophthora. However, large intraspecies synteny—compelling evidence for a WGD—has not been detected. Here, we revisited the WGD hypothesis by deducing the age of 2HOM blocks. Two independent timing methods reveal that the majority of 2HOM blocks arose after divergence of the Phytophthora lineages. In addition, a large proportion of the 2HOM block copies colocalize on the same scaffold. Therefore, the presence of 2HOM blocks does not support a WGD at the last common ancestor of Phytophthora. Thus, genome evolution of Phytophthora is likely driven by alternative mechanisms, such as bursts of transposon activity.
    Full-text · Article · Apr 2014 · Genome Biology and Evolution
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