Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides

Eukaryotic microbes have three primary mechanisms for obtaining nutrients and energy: phagotrophy, photosynthesis and osmotrophy. Traits associated with the latter two functions arose independently multiple times in the eukaryotes. The Fungi successfully coupled osmotrophy with filamentous growth, a...

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Main Authors: Leonard, G, Labarre, A, Milner, DS, Monier, A, Soanes, D, Wideman, JG, Maguire, F, Stevens, S, Sain, D, Grau-Bové, X, Sebé-Pedrós, A, Stajich, JE, Paszkiewicz, K, Brown, MW, Hall, N, Wickstead, B, Richards, TA
Format: Journal article
Language:English
Published: Royal Society 2018
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author Leonard, G
Labarre, A
Milner, DS
Monier, A
Soanes, D
Wideman, JG
Maguire, F
Stevens, S
Sain, D
Grau-Bové, X
Sebé-Pedrós, A
Stajich, JE
Paszkiewicz, K
Brown, MW
Hall, N
Wickstead, B
Richards, TA
author_facet Leonard, G
Labarre, A
Milner, DS
Monier, A
Soanes, D
Wideman, JG
Maguire, F
Stevens, S
Sain, D
Grau-Bové, X
Sebé-Pedrós, A
Stajich, JE
Paszkiewicz, K
Brown, MW
Hall, N
Wickstead, B
Richards, TA
author_sort Leonard, G
collection OXFORD
description Eukaryotic microbes have three primary mechanisms for obtaining nutrients and energy: phagotrophy, photosynthesis and osmotrophy. Traits associated with the latter two functions arose independently multiple times in the eukaryotes. The Fungi successfully coupled osmotrophy with filamentous growth, and similar traits are also manifested in the Pseudofungi (oomycetes and hyphochytriomycetes). Both the Fungi and the Pseudofungi encompass a diversity of plant and animal parasites. Genome-sequencing efforts have focused on host-associated microbes (mutualistic symbionts or parasites), providing limited comparisons with free-living relatives. Here we report the first draft genome sequence of a hyphochytriomycete ‘pseudofungus’; Hyphochytrium catenoides. Using phylogenomic approaches, we identify genes of recent viral ancestry, with related viral derived genes also present on the genomes of oomycetes, suggesting a complex history of viral coevolution and integration across the Pseudofungi. H. catenoides has a complex life cycle involving diverse filamentous structures and a flagellated zoospore with a single anterior tinselate flagellum. We use genome comparisons, drug sensitivity analysis and high-throughput culture arrays to investigate the ancestry of oomycete/pseudofungal characteristics, demonstrating that many of the genetic features associated with parasitic traits evolved specifically within the oomycete radiation. Comparative genomics also identified differences in the repertoire of genes associated with filamentous growth between the Fungi and the Pseudofungi, including differences in vesicle trafficking systems, cell-wall synthesis pathways and motor protein repertoire, demonstrating that unique cellular systems underpinned the convergent evolution of filamentous osmotrophic growth in these two eukaryotic groups.
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spelling oxford-uuid:f9959a6f-8454-4f43-8161-0d24a8b4d21f2022-03-27T12:59:07ZComparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoidesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:f9959a6f-8454-4f43-8161-0d24a8b4d21fEnglishSymplectic ElementsRoyal Society2018Leonard, GLabarre, AMilner, DSMonier, ASoanes, DWideman, JGMaguire, FStevens, SSain, DGrau-Bové, XSebé-Pedrós, AStajich, JEPaszkiewicz, KBrown, MWHall, NWickstead, BRichards, TAEukaryotic microbes have three primary mechanisms for obtaining nutrients and energy: phagotrophy, photosynthesis and osmotrophy. Traits associated with the latter two functions arose independently multiple times in the eukaryotes. The Fungi successfully coupled osmotrophy with filamentous growth, and similar traits are also manifested in the Pseudofungi (oomycetes and hyphochytriomycetes). Both the Fungi and the Pseudofungi encompass a diversity of plant and animal parasites. Genome-sequencing efforts have focused on host-associated microbes (mutualistic symbionts or parasites), providing limited comparisons with free-living relatives. Here we report the first draft genome sequence of a hyphochytriomycete ‘pseudofungus’; Hyphochytrium catenoides. Using phylogenomic approaches, we identify genes of recent viral ancestry, with related viral derived genes also present on the genomes of oomycetes, suggesting a complex history of viral coevolution and integration across the Pseudofungi. H. catenoides has a complex life cycle involving diverse filamentous structures and a flagellated zoospore with a single anterior tinselate flagellum. We use genome comparisons, drug sensitivity analysis and high-throughput culture arrays to investigate the ancestry of oomycete/pseudofungal characteristics, demonstrating that many of the genetic features associated with parasitic traits evolved specifically within the oomycete radiation. Comparative genomics also identified differences in the repertoire of genes associated with filamentous growth between the Fungi and the Pseudofungi, including differences in vesicle trafficking systems, cell-wall synthesis pathways and motor protein repertoire, demonstrating that unique cellular systems underpinned the convergent evolution of filamentous osmotrophic growth in these two eukaryotic groups.
spellingShingle Leonard, G
Labarre, A
Milner, DS
Monier, A
Soanes, D
Wideman, JG
Maguire, F
Stevens, S
Sain, D
Grau-Bové, X
Sebé-Pedrós, A
Stajich, JE
Paszkiewicz, K
Brown, MW
Hall, N
Wickstead, B
Richards, TA
Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title_full Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title_fullStr Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title_full_unstemmed Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title_short Comparative genomic analysis of the 'pseudofungus' Hyphochytrium catenoides
title_sort comparative genomic analysis of the pseudofungus hyphochytrium catenoides
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