Host-to-Pathogen Gene Transfer Facilitated Infection of Insects by a Pathogenic Fungus
The ability of infectious agents to evolve different host ranges contributes to the emergence of new diseases, and this host switching could also account for the wide variety of fungal associations with animals, plants and other fungi. There must be mechanisms for such host shifts, but these remain largely unknown. In this study, we phylogenetically predict that the endophytic fungus Metarhizium robertsii acquired a sterol carrier gene from insects through horizontal gene transfer (HGT). This sterol carrier is involved in maintaining cell membrane sterols, and thus membrane integrity, when M. robertsii proliferates in the haemocoel of living insects. Therefore, the acquisition of genetic material from a host has contributed to the development of fungal entomopathogenicity. In order to simulate this evolutionary event, the sterol carrier gene was transformed into an endophytic insect-pathogenic fungus (Beauveria bassiana) that lacks an endogenous Mr-NPC2a homolog. The virulence of B. bassiana was increased by expression of Mr-NPC2a.
Vyšlo v časopise:
Host-to-Pathogen Gene Transfer Facilitated Infection of Insects by a Pathogenic Fungus. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004009
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004009
Souhrn
The ability of infectious agents to evolve different host ranges contributes to the emergence of new diseases, and this host switching could also account for the wide variety of fungal associations with animals, plants and other fungi. There must be mechanisms for such host shifts, but these remain largely unknown. In this study, we phylogenetically predict that the endophytic fungus Metarhizium robertsii acquired a sterol carrier gene from insects through horizontal gene transfer (HGT). This sterol carrier is involved in maintaining cell membrane sterols, and thus membrane integrity, when M. robertsii proliferates in the haemocoel of living insects. Therefore, the acquisition of genetic material from a host has contributed to the development of fungal entomopathogenicity. In order to simulate this evolutionary event, the sterol carrier gene was transformed into an endophytic insect-pathogenic fungus (Beauveria bassiana) that lacks an endogenous Mr-NPC2a homolog. The virulence of B. bassiana was increased by expression of Mr-NPC2a.
Zdroje
1. VoylesJ, YoungS, BergerL, CampbellC, VoylesWF, et al. (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326(5952): 582–585.
2. LorchJM, MeteyerCU, BehrMJ, BoylesJG, CryanPM, et al. (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480(7377): 376–378.
3. SuhSO, NodaH, BlackwellM (2001) Insect symbiosis: derivation of yeast-like endosymbionts within an entomopathogenic filamentous lineage. Mol Biol Evol 18(6): 995–1000.
4. RicklefsRE, FallonSM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci 269: 885–892.
5. ArchieEA, LuikartG, EzenwaVO (2009) Infecting epidemiology with genetics: a new frontier in disease ecology. Trends Ecol Evol 24: 21–30.
6. RaffaeleS, FarrerRA, CanoLM, StudholmeDJ, MacLeanD, et al. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540–1543.
7. GilbertC, HernandezSS, Flores-BenabibJ, SmithEN, FeschotteC (2012) Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol Biol Evol 29: 503–515.
8. SlotJC, RokasA (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21(2): 134–139.
9. FriesenTL, StukenbrockEH, LiuZ, MeinhardtS, LingH, et al. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953–956.
10. RichardsTA, LeonardG, SoanesDM, TalbotNJ (2011) Gene transfer into the fungi. Fungal. Biol Rev 25: 98–110.
11. SunBF, XiaoJH, HeS, LiuL, MurphyRW, et al. (2013) Multiple interkingdom horizontal gene transfers in Pyrenophora and closely related species and their contributions to phytopathogenic lifestyles. PLoS One 8(3): e60029.
12. MowerJP, StefanovicS, YoungGJ, PalmerJD (2004) Plant genetics: gene transfer from parasitic to host plants. Nature 432: 165–166.
13. DavisCC, WurdackKJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305: 676–678.
14. KeelingPJ, PalmerJD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605–618.
15. SelmanM, PombertJF, SolterL, FarinelliL, WeissLM, et al. (2011) Acquisition of an animal gene by microsporidian intracellular parasites. Curr Biol 21: 576–577.
16. BarDZ (2011) Evidence of massive horizontal gene transfer between humans and Plasmodium vivax. Nature precedings doi:10.1038/npre.2011.5690.1
17. RobertsDW, St LegerRJ (2004) Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv Appl Microbiol 54: 1–70.
18. FangW, ScullyLR, ZhangL, PeiY, BidochkaMJ (2008) Implication of a regulator of G protein signalling (BbRGS1) in conidiation and conidial thermotolerance of the insect pathogenic fungus Beauveria bassiana. FEMS Microbiol Lett 279: 146–156.
19. FangW, AzimzadehP, St LegerRJ (2012) Strain improvement of fungal insecticides for controlling insect pests and vector-borne diseases. Curr Opin Microbiol 15: 232–238.
20. BehieSW, ZeliskoPM, BidochkaMJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336: 1576–1577.
21. FangW, St LegerRJ (2010) Mrt, a gene unique to fungi, encodes an oligosaccharide transporter and facilitates rhizosphere competency in Metarhizium robertsii. Plant Physiol 154: 1549–1557.
22. XiaoG, YingSH, ZhengP, WangZL, ZhangS, et al. (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2: 483.
23. FangW, FernandesEK, RobertsDW, BidochkaMJ, St LegerRJ (2010) A laccase exclusively expressed by Metarhizium anisopliae during isotropic growth is involved in pigmentation, tolerance to abiotic stresses and virulence. Fungal Genet Biol 47: 602–607.
24. ShimodairaH, HasegawaM (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17(12): 1246–1247.
25. ButlerMD, AldermanSC, HammondPC, BerryRE (2001) Association of Insects and Ergot (Claviceps purpurea) in Kentucky Bluegrass Seed Production Fields. J Econ Entomol 94: 1471–1476.
26. DanchinEG, RossoMN, VieiraP, de Almeida-EnglerJ, CoutinhoPM, et al. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107(41): 17651–17656.
27. ShiXZ, ZhongX, YuXQ (2012) Drosophila melanogaster NPC2 proteins bind bacterial cell wall components and may function in immune signal pathways. Insect Biochem Mol Biol 42: 545–556.
28. BergerAC, VanderfordTH, GernertKM, NicholsJW, FaundezV, et al. (2005) Saccharomyces cerevisiae Npc2p is a functionally conserved homologue of the human Niemann-Pick disease type C 2 protein, hNPC2. Eukaryot Cell 4: 1851–1862.
29. WangC, St LegerRJ (2006) A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc Natl Acad Sci USA 103: 6647–6652.
30. McCluskeyK (2003) The Fungal Genetics Stock Center: from molds to molecules. Adv Appl Microbiol 52: 245–262.
31. ChenP, GaoR, ChenS, PuL, LiP, et al. (2012) A pericentrin-related protein homolog in Aspergillus nidulans plays important roles in nucleus positioning and cell polarity by affecting microtubule organization. Eukaryot Cell 11: 1520–1530.
32. GerphagnonM, LatourD, ColombetJ, Sime-NgandoT (2013) A double staining method using SYTOX green and calcofluor white for studying fungal parasites of phytoplankton. Appl Environ Microbiol 79: 3943–3951.
33. HorbachR, Navarro-QuesadaAR, KnoggeW, DeisingHB (2011) When and how to kill a plant cell: infection strategies of plant pathogenic fungi. J Plant Physiol 168: 51–62.
34. GardinerDM, KazanK, MannersJM (2013) Cross-kingdom gene transfer facilitates the evolution of virulence in fungal pathogens. Plant Sci 210: 151–158.
35. ZhangYQ, GamarraS, Garcia-EffronG, ParkS, PerlinDS, et al. (2010) Requirement for ergosterol in V-ATPase function underlies antifungal activity of azole drugs. PLoS Pathog 6: e1000939.
36. DupontS, LemetaisG, FerreiraT, CayotP, GervaisP, et al. (2012) Ergosterol biosynthesis: a fungal pathway for life on land? Evolution 66: 2961–2968.
37. AndreasenAA, StierTJ (1953) Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J Cell Physiol 41: 23–36.
38. JingX, GrebenokRJ, BehmerST (2013) Sterol/steroid metabolism and absorption in a generalist and specialist caterpillar: Effects of dietary sterol/steroid structure, mixture and ratio. Insect Biochem Mol Biol 43: 580–587.
39. JacquierN, SchneiterR (2012) Mechanisms of sterol uptake and transport in yeast. J Steroid Biochem Mol Biol 129: 70–78.
40. XiongQ, HassanSA, WilsonWK, HanXY, MayGS, et al. (2005) Cholesterol import by Aspergillus fumigatus and its influence on antifungal potency of sterol biosynthesis inhibitors. Antimicrob Agents Chemother 49: 518–524.
41. AlimardaniP, RegnacqM, Moreau-VauzelleC, FerreiraT, RossignolT, et al. (2004) SUT1-promoted sterol uptake involves the ABC transporter Aus1 and the mannoprotein Dan1 whose synergistic action is sufficient for this process. Biochem J 381: 195–202.
42. BergerAC, HansonPK, Wylie NicholsJ, CorbettAH (2005) A yeast model system for functional analysis of the Niemann-Pick type C protein 1 homolog, Ncr1p. Traffic 6: 907–917.
43. BischoffJF, RehnerSA, HumberRA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 101: 512–530.
44. FangW, PeiY, BidochkaMJ (2007) A regulator of a G protein signaling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation, virulence and hydrophobin synthesis. Microbiology 153: 1017–1025.
45. FangW, PeiY, BidochkaMJ (2006) Transformation of Metarhizium anisopliae mediated by Agrobacterium tumefaciens. Can J Microbiol 52: 623–626.
46. FangW, LengB, XiaoY, JinK, MaJ, et al. (2005) Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Appl Environ Microbiol 71: 363–370.
47. FangW, St LegerRJ (2012) Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi. PLoS One 7: e43069.
48. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
49. CastresanaJ (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552.
50. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.
51. AbascalF, ZardoyaR, PosadaD (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.
52. HuelsenbeckJP, RonquistF (2001) MR BAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
53. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
54. FangW, BidochkaMJ (2006) Expression of genes involved in germination, conidiogenesis and pathogenesis in Metarhizium anisopliae using quantitative real-time RT-PCR. Mycol Res 110: 1165–1171.
55. FangW, Pava-ripollM, WangS, St.LegerRJ (2009) Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Genet Biol 46: 277–85.
56. FangW, FengJ, FanY, ZhangY, BidochkaMJ, et al. (2009) Expressing a fusion protein with protease and chitinase activities increases the virulence of the insect pathogen Beauveria bassiana. J Invertebr Pathol 102: 155–159.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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