title: Transcriptome analysis of the entomopathogenic oomycete Lagenidium giganteum reveals putative virulence factors.
abstract: A combination of 454 pyrosequencing and Sanger sequencing was used to sample and characterize the transcriptome of the entomopathogenic oomycete Lagenidium giganteum. More than 50,000 high-throughput reads were annotated through homology searches. Several selected reads served as seeds for the amplification and sequencing of full-length transcripts. Phylogenetic analyses inferred from full-length cellulose synthase alignments revealed that L giganteum is nested within the peronosporalean galaxy and as such appears to have evolved from a phytopathogenic ancestor. In agreement with the phylogeny reconstructions, full-length L. giganteum oomycete effector orthologs, corresponding to the cellulose-binding elicitor lectin (CBEL), crinkler (CRN), and elicitin proteins, were characterized by domain organizations similar to those of pathogenicity factors of plant-pathogenic oomycetes. Importantly, the L. giganteum effectors provide a basis for detailing the roles of canonical CRN, CBEL, and elicitin proteins in the infectious process of an oomycete known principally as an animal pathogen. Finally, phylogenetic analyses and genome mining identified members of glycoside hydrolase family 5 subfamily 27 (GH5_27) as putative virulence factors active on the host insect cuticle, based in part on the fact that GH5_27 genes are shared by entomopathogenic oomycetes and fungi but are underrepresented in nonentomopathogenic genomes. The genomic resources gathered from the L. giganteum transcriptome analysis strongly suggest that filamentous entomopathogens (oomycetes and fungi) exhibit convergent evolution: they have evolved independently from plant-associated microbes, have retained genes indicative of plant associations, and may share similar cores of virulence factors, such as GH5_27 enzymes, that are absent from the genomes of their plant-pathogenic relatives.
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Paula F
authors.initials: PF
authors.lastname: Quiroz Velasquez
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Sumayyah K
authors.initials: SK
authors.lastname: Abiff
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Katrina C
authors.initials: KC
authors.lastname: Fins
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Quincy B
authors.initials: QB
authors.lastname: Conway
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Norma C
authors.initials: NC
authors.lastname: Salazar
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Ana Paula
authors.initials: AP
authors.lastname: Delgado
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Jhanelle K
authors.initials: JK
authors.lastname: Dawes
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA.
authors.forename: Lauren G
authors.initials: LG
authors.lastname: Douma
authors.affiliation: Division of Math Science and Technology, Nova Southeastern University, Fort Lauderdale, Florida, USA aurelien@nova.edu.
authors.forename: Aurélien
authors.initials: A
authors.lastname: Tartar
mesh_terms: D000818:Animals; D009033:Culicidae / Q000382:microbiology; D005656:Fungal Proteins / Q000235:genetics; D005964:Glucosyltransferases / Q000235:genetics; D054884:Host-Pathogen Interactions / Q000235:genetics; D044726:Lagenidium / Q000235:genetics* / Q000472:pathogenicity*; D008969:Molecular Sequence Data; D010802:Phylogeny; D059467:Transcriptome; D037521:Virulence Factors / Q000235:genetics*
chemical_list: D005656:Fungal Proteins; D037521:Virulence Factors; D005964:Glucosyltransferases; C478648:cellulose synthase
references.citation: J Econ Entomol. 1990 Apr;83(2):374-6
references.pmid: 2345220
references.citation: BMC Genomics. 2012 Nov 09;13:605
references.pmid: 23140525
references.citation: Nat Methods. 2012 Jul 30;9(8):772
references.pmid: 22847109
references.citation: Insects. 2013 Jul 16;4(3):357-74
references.pmid: 26462424
references.citation: Curr Genet. 2007 Sep;52(3-4):115-23
references.pmid: 17661047
references.citation: Sci Rep. 2012;2:483
references.pmid: 22761991
references.citation: Proc Natl Acad Sci U S A. 2010 Oct 5;107(40):17421-6
references.pmid: 20847293
references.citation: J Med Entomol. 1988 Nov;25(6):452-60
references.pmid: 3204624
references.citation: Curr Genet. 2012 Dec;58(5-6):265-79
references.pmid: 23052419
references.citation: Appl Microbiol Biotechnol. 2013 Apr;97(7):2797-804
references.pmid: 23435902
references.citation: J Invertebr Pathol. 1989 Jul;54(1):103-11
references.pmid: 2567775
references.citation: Fungal Biol. 2012 Apr;116(4):529-42
references.pmid: 22483051
references.citation: Genome Biol. 2011 Nov 23;12(11):R116
references.pmid: 22112802
references.citation: J Am Mosq Control Assoc. 2007;23(2 Suppl):50-7
references.pmid: 17853597
references.citation: BMC Evol Biol. 2011 Jul 08;11:195
references.pmid: 21740557
references.citation: Genome Biol. 2010;11(7):R73
references.pmid: 20626842
references.citation: Fungal Biol. 2012 Jan;116(1):24-41
references.pmid: 22208599
references.citation: J Econ Entomol. 1988 Feb;81(1):158-71
references.pmid: 3351077
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: Fungal Genet Biol. 2006 Jan;43(1):20-33
references.pmid: 16380277
references.citation: J Am Mosq Control Assoc. 2000 Mar;16(1):5-8
references.pmid: 10757483
references.citation: J Proteome Res. 2014 May 2;13(5):2282-96
references.pmid: 24702058
references.citation: Phytopathology. 2013 Oct;103(10):1035-44
references.pmid: 23634808
references.citation: Cell Microbiol. 2009 Jan;11(1):13-20
references.pmid: 18783481
references.citation: PLoS One. 2013;8(3):e59357
references.pmid: 23516629
references.citation: Nucleic Acids Res. 2009 Jan;37(Database issue):D233-8
references.pmid: 18838391
references.citation: Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W465-9
references.pmid: 18424797
references.citation: Curr Opin Plant Biol. 2011 Aug;14(4):407-14
references.pmid: 21641854
references.citation: J Invertebr Pathol. 2002 Jun;80(2):112-26
references.pmid: 12383436
references.citation: BMC Evol Biol. 2012 Sep 20;12:186
references.pmid: 22992189
references.citation: Bioinformatics. 2005 May 1;21(9):2104-5
references.pmid: 15647292
references.citation: J Vet Intern Med. 2003 Sep-Oct;17(5):637-46
references.pmid: 14529129
references.citation: J Invertebr Pathol. 2008 Sep;99(1):96-102
references.pmid: 18433768
references.citation: Mol Biol Evol. 2006 May;23(5):1048-55
references.pmid: 16495348
references.citation: J Am Mosq Control Assoc. 1994 Sep;10(3):451-5
references.pmid: 7807095
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D675-81
references.pmid: 22064857
references.citation: BMC Bioinformatics. 2006 Oct 10;7:439
references.pmid: 17032440
references.citation: Am J Vet Res. 2009 Feb;70(2):163; author reply 163
references.pmid: 19231944
references.citation: PLoS Genet. 2014 May 08;10(5):e1004355
references.pmid: 24809511
references.citation: Genome Res. 2004 Jun;14(6):1188-90
references.pmid: 15173120
references.citation: Insect Mol Biol. 2006 Oct;15(5):715-8
references.pmid: 17069642
references.citation: BMC Genomics. 2008 Nov 15;9:542
references.pmid: 19014603
references.citation: Bioinformatics. 2005 Sep 15;21(18):3674-6
references.pmid: 16081474
references.citation: Curr Opin Plant Biol. 2012 Aug;15(4):483-92
references.pmid: 22483402
references.citation: Protoplasma. 2012 Jan;249(1):3-19
references.pmid: 21424613
references.citation: Mol Plant Pathol. 2012 May;13(4):414-30
references.pmid: 22471698
references.citation: Fungal Biol. 2011 Jul;115(7):683-96
references.pmid: 21724174
references.citation: J Biol Chem. 2000 Oct 6;275(40):31297-304
references.pmid: 10882727
references.citation: J AAPOS. 2011 Feb;15(1):101-3
references.pmid: 21316282
references.citation: J Insect Sci. 2004;4:19
references.pmid: 15861235
references.citation: Antonie Van Leeuwenhoek. 1976;42(1-2):131-9
references.pmid: 1085124
references.citation: PLoS Genet. 2013 Jun;9(6):e1003272
references.pmid: 23785293
references.citation: Genome Res. 1999 Sep;9(9):868-77
references.pmid: 10508846
references.citation: J Econ Entomol. 1987 Oct;80(5):994-7
references.pmid: 2891737
references.citation: Mol Biol Evol. 2006 Feb;23(2):338-51
references.pmid: 16237208
references.citation: J Clin Microbiol. 2013 Aug;51(8):2778-80
references.pmid: 23740721
references.citation: J Invertebr Pathol. 1994 Nov;64(3):228-33
references.pmid: 7806894
references.citation: PLoS Biol. 2014 Feb 25;12(2):e1001801
references.pmid: 24586116
references.citation: Mycopathologia. 2006 Feb;161(2):109-18
references.pmid: 16463094
references.citation: Nat Biotechnol. 2013 Nov;31(11):1009-14
references.pmid: 24108091
references.citation: Curr Biol. 2006 Sep 19;16(18):1857-64
references.pmid: 16979565
references.citation: Nat Rev Microbiol. 2006 Dec;4(12):922-31
references.pmid: 17088934
references.citation: PLoS Genet. 2011 Jan 06;7(1):e1001264
references.pmid: 21253567
references.citation: Eur J Ophthalmol. 2012 Sep-Oct;22(5):814-8
references.pmid: 22467587
references.citation: Trends Microbiol. 2003 Oct;11(10):462-9
references.pmid: 14557029
references.citation: PLoS One. 2013;8(3):e59517
references.pmid: 23536880
references.citation: Syst Biol. 2010 May;59(3):307-21
references.pmid: 20525638
references.citation: Trends Microbiol. 2008 Jan;16(1):13-9
references.pmid: 18096392
references.citation: Annu Rev Phytopathol. 2006;44:41-60
references.pmid: 16448329