Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica

Rays H Y Jiang, Irene de Bruijn, Brian J Haas, Rodrigo Belmonte, Lars Löbach, James Christie, Guido van den Ackerveken, Arnaud Bottin, Vincent Bulone, Sara M Díaz-Moreno, Bernard Dumas, Lin Fan, Elodie Gaulin, Francine Govers, Laura J Grenville-Briggs, Neil R Horner, Joshua Z Levin, Marco Mammella, Harold J G Meijer, Paul Morris & 21 others Chad Nusbaum, Stan Oome, Andrew J Phillips, David van Rooyen, Elzbieta Rzeszutek, Marcia Saraiva, Chris J Secombes, Michael F Seidl, Berend Snel, Joost H M Stassen, Sean Sykes, Sucheta Tripathy, Herbert van den Berg, Julio C Vega-Arreguin, Stephan Wawra, Sarah K Young, Qiandong Zeng, Javier Dieguez-Uribeondo, Carsten Russ, Brett M Tyler, Pieter van West

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Abstract

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.
Original languageEnglish
Article numbere1003272
Number of pages20
JournalPLoS Genetics
Volume9
Issue number6
DOIs
Publication statusPublished - 13 Jun 2013

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Saprolegnia
Saprolegnia parasitica
Oomycetes
virulence
Virulence
Fishes
genome
pathogen
Genome
gene
pathogens
fish
animal
Genes
genes
animal pathogens
Galectins
Phytophthora
Disintegrins
Plant Genome

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Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. / Jiang, Rays H Y; de Bruijn, Irene; Haas, Brian J; Belmonte, Rodrigo; Löbach, Lars; Christie, James; van den Ackerveken, Guido; Bottin, Arnaud; Bulone, Vincent; Díaz-Moreno, Sara M; Dumas, Bernard; Fan, Lin; Gaulin, Elodie; Govers, Francine; Grenville-Briggs, Laura J; Horner, Neil R; Levin, Joshua Z; Mammella, Marco; Meijer, Harold J G; Morris, Paul; Nusbaum, Chad; Oome, Stan; Phillips, Andrew J; van Rooyen, David; Rzeszutek, Elzbieta; Saraiva, Marcia; Secombes, Chris J; Seidl, Michael F; Snel, Berend; Stassen, Joost H M; Sykes, Sean; Tripathy, Sucheta; van den Berg, Herbert; Vega-Arreguin, Julio C; Wawra, Stephan; Young, Sarah K; Zeng, Qiandong; Dieguez-Uribeondo, Javier; Russ, Carsten; Tyler, Brett M; van West, Pieter.

In: PLoS Genetics, Vol. 9, No. 6, e1003272, 13.06.2013.

Research output: Contribution to journalArticle

Jiang, RHY, de Bruijn, I, Haas, BJ, Belmonte, R, Löbach, L, Christie, J, van den Ackerveken, G, Bottin, A, Bulone, V, Díaz-Moreno, SM, Dumas, B, Fan, L, Gaulin, E, Govers, F, Grenville-Briggs, LJ, Horner, NR, Levin, JZ, Mammella, M, Meijer, HJG, Morris, P, Nusbaum, C, Oome, S, Phillips, AJ, van Rooyen, D, Rzeszutek, E, Saraiva, M, Secombes, CJ, Seidl, MF, Snel, B, Stassen, JHM, Sykes, S, Tripathy, S, van den Berg, H, Vega-Arreguin, JC, Wawra, S, Young, SK, Zeng, Q, Dieguez-Uribeondo, J, Russ, C, Tyler, BM & van West, P 2013, 'Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica', PLoS Genetics, vol. 9, no. 6, e1003272. https://doi.org/10.1371/journal.pgen.1003272
Jiang, Rays H Y ; de Bruijn, Irene ; Haas, Brian J ; Belmonte, Rodrigo ; Löbach, Lars ; Christie, James ; van den Ackerveken, Guido ; Bottin, Arnaud ; Bulone, Vincent ; Díaz-Moreno, Sara M ; Dumas, Bernard ; Fan, Lin ; Gaulin, Elodie ; Govers, Francine ; Grenville-Briggs, Laura J ; Horner, Neil R ; Levin, Joshua Z ; Mammella, Marco ; Meijer, Harold J G ; Morris, Paul ; Nusbaum, Chad ; Oome, Stan ; Phillips, Andrew J ; van Rooyen, David ; Rzeszutek, Elzbieta ; Saraiva, Marcia ; Secombes, Chris J ; Seidl, Michael F ; Snel, Berend ; Stassen, Joost H M ; Sykes, Sean ; Tripathy, Sucheta ; van den Berg, Herbert ; Vega-Arreguin, Julio C ; Wawra, Stephan ; Young, Sarah K ; Zeng, Qiandong ; Dieguez-Uribeondo, Javier ; Russ, Carsten ; Tyler, Brett M ; van West, Pieter. / Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. In: PLoS Genetics. 2013 ; Vol. 9, No. 6.
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abstract = "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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T1 - Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica

AU - Jiang, Rays H Y

AU - de Bruijn, Irene

AU - Haas, Brian J

AU - Belmonte, Rodrigo

AU - Löbach, Lars

AU - Christie, James

AU - van den Ackerveken, Guido

AU - Bottin, Arnaud

AU - Bulone, Vincent

AU - Díaz-Moreno, Sara M

AU - Dumas, Bernard

AU - Fan, Lin

AU - Gaulin, Elodie

AU - Govers, Francine

AU - Grenville-Briggs, Laura J

AU - Horner, Neil R

AU - Levin, Joshua Z

AU - Mammella, Marco

AU - Meijer, Harold J G

AU - Morris, Paul

AU - Nusbaum, Chad

AU - Oome, Stan

AU - Phillips, Andrew J

AU - van Rooyen, David

AU - Rzeszutek, Elzbieta

AU - Saraiva, Marcia

AU - Secombes, Chris J

AU - Seidl, Michael F

AU - Snel, Berend

AU - Stassen, Joost H M

AU - Sykes, Sean

AU - Tripathy, Sucheta

AU - van den Berg, Herbert

AU - Vega-Arreguin, Julio C

AU - Wawra, Stephan

AU - Young, Sarah K

AU - Zeng, Qiandong

AU - Dieguez-Uribeondo, Javier

AU - Russ, Carsten

AU - Tyler, Brett M

AU - van West, Pieter

PY - 2013/6/13

Y1 - 2013/6/13

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pgen.1003272

DO - 10.1371/journal.pgen.1003272

M3 - Article

VL - 9

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 6

M1 - e1003272

ER -